Running, swimming and diving modifies neuroprotecting globins in the mammalian brain.
The vulnerability of the human brain to injury following just a few minutes of oxygen deprivation with submergence contrasts markedly with diving mammals, such as Weddell seals (Leptonychotes weddellii), which can remain underwater for more than 90 min while exhibiting no neurological or behavioural impairment. This response occurs despite exposure to blood oxygen levels concomitant with human unconsciousness. To determine whether such aquatic lifestyles result in unique adaptations for avoiding ischaemic-hypoxic neural damage, we measured the presence of circulating (haemoglobin) and resident (neuroglobin and cytoglobin) oxygen-carrying globins in the cerebral cortex of 16 mammalian species considered terrestrial, swimming or diving specialists. Here we report a striking difference in globin levels depending on activity lifestyle. A nearly 9.5-fold range in haemoglobin concentration (0.17-1.62 g Hb 100 g brain wet wt(-1)) occurred between terrestrial and deep-diving mammals; a threefold range in resident globins was evident between terrestrial and swimming specialists. Together, these two globin groups provide complementary mechanisms for facilitating oxygen transfer into neural tissues and the potential for protection against reactive oxygen and nitrogen groups. This enables marine mammals to maintain sensory and locomotor neural functions during prolonged submergence, and suggests new avenues for averting oxygen-mediated neural injury in the mammalian brain.
Williams
Terrie M
TM
Department of Ecology and Evolutionary Biology, Center for Ocean Health-Long Marine Laboratory, University of California at Santa Cruz, 100 Shaffer Road, Santa Cruz, CA 95060, USA. williams@biology.ucsc.edu
Zavanelli
Mary
M
Miller
Melissa A
MA
Goldbeck
Robert A
RA
Morledge
Michael
M
Casper
Dave
D
Pabst
D Ann
DA
McLellan
William
W
Cantin
Lucas P
LP
Kliger
David S
DS
D000818:Animals; D002335:Carnivora / Q000378:metabolism / Q000502:physiology*; D002540:Cerebral Cortex / Q000378:metabolism*; D002591:Cetacea / Q000378:metabolism / Q000502:physiology*; D000078842:Cytoglobin; D004242:Diving / Q000502:physiology; D005914:Globins / Q000235:genetics / Q000378:metabolism*; D006454:Hemoglobins / Q000235:genetics / Q000378:metabolism*; D006801:Humans; D000860:Hypoxia / Q000517:prevention & control; D007511:Ischemia / Q000517:prevention & control; D051379:Mice; D009419:Nerve Tissue Proteins / Q000235:genetics / Q000378:metabolism*; D000078787:Neuroglobin; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D012420:Running / Q000502:physiology; D013550:Swimming / Q000502:physiology
C000627265:CYGB protein, human; C000627267:Cygb protein, mouse; D000078842:Cytoglobin; D006454:Hemoglobins; D009419:Nerve Tissue Proteins; D000078787:Neuroglobin; D012333:RNA, Messenger; D005914:Globins