Sex-dependent mitochondrial respiratory impairment and oxidative stress in a rat model of neonatal hypoxic-ischemic encephalopathy

Journal of Neurochemistry

Volumn 137, Issue 5, 2016, Pages 714-729

  Demarest, Tyler G ^a   Schuh, Rosemary A ^a   Waddell, Jaylyn ^a   McKenna, Mary C ^a   Fiskum, Gary ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

glutathione; glutathione peroxidase; oxidative phosphorylation; protein carbonyl

Indexed keywords

GLUTATHIONE; GLUTATHIONE PEROXIDASE; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DISEASE PREDISPOSITION; DISEASE SEVERITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; FEMALE; HIPPOCAMPUS; HYPOXIC ISCHEMIC ENCEPHALOPATHY; MALE; MITOCHONDRIAL RESPIRATION; NEWBORN; NEWBORN DISEASE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PERIRHINAL CORTEX; PRIORITY JOURNAL; PROTEIN CARBONYLATION; RAT; RAT MODEL; SEX DIFFERENCE; ANIMAL; DISEASE MODEL; METABOLISM; MITOCHONDRION; OXYGEN CONSUMPTION; PATHOLOGY; PHYSIOLOGY; SEXUAL DEVELOPMENT; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; FEMALE; HYPOXIA-ISCHEMIA, BRAIN; MALE; MITOCHONDRIA; OXIDATIVE STRESS; OXYGEN CONSUMPTION; RATS; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS;

EID: 84966400933     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13590     Document Type: Article

References (67)

1. Barker G. R., and, Warburton E. C., (2011) When is the hippocampus involved in recognition memory? J. Neurosci. 31, 10721-10731.
2. Bayir H., Adelson P. D., Wisniewski S. R., Shore P., Lai Y., Brown D., Janesko-Feldman K. L., Kagan V. E., and, Kochanek P. M., (2009) Therapeutic hypothermia preserves antioxidant defenses after severe traumatic brain injury in infants and children. Crit. Care Med. 37, 689-695.
3. Black S. M., Bedolli M. A., Martinez S., Bristow J. D., Ferriero D. M., and, Soifer S. J., (1995) Expression of neuronal nitric oxide synthase corresponds to regions of selective vulnerability to hypoxia-ischaemia in the developing rat brain. Neurobiol. Dis. 2, 145-155.
4. Blomgren K., and, Hagberg H., (2006) Free radicals, mitochondria, and hypoxia-ischemia in the developing brain. Free Radic. Biol. Med. 40, 388-397.
5. Blomgren K., Zhu C., Hallin U., and, Hagberg H., (2003) Mitochondria and ischemic reperfusion damage in the adult and in the developing brain. Biochem. Biophys. Res. Commun. 304, 551-559.
6. Brown G. C., (2000) Nitric oxide as a competitive inhibitor of oxygen consumption in the mitochondrial respiratory chain. Acta Physiol. Scand. 168, 667-674.
7. Davidson J. O., Wassink G., van den Heuij L. G., Bennet L., and, Gunn A. J., (2015) Therapeutic hypothermia for neonatal hypoxic-ischemic encephalopathy-Where to from here? Front. Neurol. 6, 198.
8. Deierborg T., Wieloch T., Diano S., Warden C. H., Horvath T. L., and, Mattiasson G., (2008) Overexpression of UCP2 protects thalamic neurons following global ischemia in the mouse. J. Cereb. Blood Flow Metab. 28, 1186-1195.
9. Dell'Anna E., Iuvone L., Calzolari S., and, Geloso M. C., (1997) Effect of acetyl-L-carnitine on hyperactivity and spatial memory deficits of rats exposed to neonatal anoxia. Neurosci. Lett. 223, 201-205.
10. Demarest T. G., and, McCarthy M. M., (2015) Sex differences in mitochondrial (dys)function: implications for neuroprotection. J. Bioenerg. Biomembr. 47, 173-188.
11. Ditelberg J. S., Sheldon R. A., Epstein C. J., and, Ferriero D. M., (1996) Brain injury after perinatal hypoxia-ischemia is exacerbated in copper/zinc superoxide dismutase transgenic mice. Pediatr. Res. 39, 204-208.
12. Du L., Bayir H., Lai Y., Zhang X., Kochanek P. M., Watkins S. C., Graham S. H., and, Clark R. S., (2004) Innate gender-based proclivity in response to cytotoxicity and programmed cell death pathway. J. Biol. Chem. 279, 38563-38570.
13. Echtay K. S., Roussel D., St-Pierre J., et al,. (2002) Superoxide activates mitochondrial uncoupling proteins. Nature 415, 96-99.
14. Ferriero D. M., (2001) Oxidant mechanisms in neonatal hypoxia-ischemia. Dev. Neurosci. 23, 198-202.
15. Ferriero D. M., Holtzman D. M., Black S. M., and, Sheldon R. A., (1996) Neonatal mice lacking neuronal nitric oxide synthase are less vulnerable to hypoxic-ischemic injury. Neurobiol. Dis. 3, 64-71.
16. Fiskum G., (2000) Mitochondrial participation in ischemic and traumatic neural cell death. J. Neurotrauma 17, 843-855.
17. Goo M. J., Choi S. M., Kim S. H., and, Ahn B. O., (2012) Protective effects of acetyl-L-carnitine on neurodegenarative changes in chronic cerebral ischemia models and learning-memory impairment in aged rats. Arch. Pharm. Res. 35, 145-154.
18. Gulcan H., Ozturk I. C., and, Arslan S., (2005) Alterations in antioxidant enzyme activities in cerebrospinal fluid related with severity of hypoxic ischemic encephalopathy in newborns. Biol. Neonate 88, 87-91.
19. Hagberg H., Mallard C., Rousset C. I., and, Xiaoyang W., (2009) Apoptotic mechanisms in the immature brain: involvement of mitochondria. J. Child Neurol. 24, 1141-1146.
20. Hagberg H., Mallard C., Rousset C. I., and, Thornton C., (2014) Mitochondria: hub of injury responses in the developing brain. Lancet Neurol. 13, 217-232.
21. Haynes R. L., Baud O., Li J., Kinney H. C., Volpe J. J., and, Folkerth D. R., (2005) Oxidative and nitrative injury in periventricular leukomalacia: a review. Brain Pathol. 15, 225-233.
22. Hill C. A., and, Fitch R. H., (2012) Sex differences in mechanisms and outcome of neonatal hypoxia-ischemia in rodent models: implications for sex-specific neuroprotection in clinical neonatal practice. Neurol. Res. Int. 2012, 867531.
23. Jones L. L., McDonald D. A., and, Borum P. R., (2010) Acylcarnitines: role in brain. Prog. Lipid Res. 49, 61-75.
24. Konkle A. T., and, McCarthy M. M., (2011) Developmental time course of estradiol, testosterone, and dihydrotestosterone levels in discrete regions of male and female rat brain. Endocrinology 152, 223-235.
25. Korde A. S., Pettigrew L. C., Craddock S. D., and, Maragos W. F., (2005) The mitochondrial uncoupler 2,4-dinitrophenol attenuates tissue damage and improves mitochondrial homeostasis following transient focal cerebral ischemia. J. Neurochem. 94, 1676-1684.
26. Korshunov S. S., Korkina O. V., Ruuge E. K., Skulachev V. P., and, Starkov A. A., (1998) Fatty acids as natural uncouplers preventing generation of O2.- and H2O2 by mitochondria in the resting state. FEBS Lett. 435, 215-218.
27. Kurinczuk J. J., White-Koning M., and, Badawi N., (2010) Epidemiology of neonatal encephalopathy and hypoxic-ischaemic encephalopathy. Early Hum. Dev. 86, 329-338.
28. Lazarus R. C., Buonora J. E., Jacobowitz D. M., and, Mueller G. P., (2015) Protein carbonylation after traumatic brain injury: cell specificity, regional susceptibility, and gender differences. Free Radic. Biol. Med. 78, 89-100.
29. Liu Y., Rosenthal R. E., Starke-Reed P., and, Fiskum G., (1993) Inhibition of postcardiac arrest brain protein oxidation by acetyl-L-carnitine. Free Radic. Biol. Med. 15, 667-670.
30. Mbemba F., Houbion A., Raes M., and, Remacle J., (1985) Subcellular localization and modification with ageing of glutathione, glutathione peroxidase and glutathione reductase activities in human fibroblasts. Biochim. Biophys. Acta 838, 211-220.
31. McCullough L. D., Zeng Z., Blizzard K. K., Debchoudhury I., and, Hurn P. D., (2005) Ischemic nitric oxide and poly (ADP-ribose) polymerase-1 in cerebral ischemia: male toxicity, female protection. J. Cereb. Blood Flow Metab. 25, 502-512.
32. Mendez M., Arias N., Uceda S., and, Arias J. L., (2015) c-Fos expression correlates with performance on novel object and novel place recognition tests. Brain Res. Bull. 117, 16-23.
33. Morken T. S., Brekke E., Haberg A., Wideroe M., Brubakk A. M., and, Sonnewald U., (2014) Altered astrocyte-neuronal interactions after hypoxia-ischemia in the neonatal brain in female and male rats. Stroke 45, 2777-2785.
34. Mueller-Burke D., Koehler R. C., and, Martin L. J., (2008) Rapid NMDA receptor phosphorylation and oxidative stress precede striatal neurodegeneration after hypoxic ischemia in newborn piglets and are attenuated with hypothermia. Int. J. Dev. Neurosci. 26, 67-76.
35. Niatsetskaya Z. V., Sosunov S. A., Matsiukevich D., Utkina-Sosunova I. V., Ratner V. I., Starkov A. A., and, Ten V. S., (2012) The oxygen free radicals originating from mitochondrial complex I contribute to oxidative brain injury following hypoxia-ischemia in neonatal mice. J. Neurosci. 32, 3235-3244.
36. Okado-Matsumoto A., and, Fridovich I., (2001) Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu, Zn-SOD in mitochondria. J. Biol. Chem. 276, 38388-38393.
37. Olesen K. M., and, Auger A. P., (2005) Sex differences in Fos protein expression in the neonatal rat brain. J. Neuroendocrinol. 17, 255-261.
38. Patel S. P., Sullivan P. G., Lyttle T. S., Magnuson D. S., and, Rabchevsky A. G., (2012) Acetyl-L-carnitine treatment following spinal cord injury improves mitochondrial function correlated with remarkable tissue sparing and functional recovery. Neuroscience 210, 296-307.
39. Puka-Sundvall M., Wallin C., Gilland E., Hallin U., Wang X., Sandberg M., Karlsson J., Blomgren K., and, Hagberg H., (2000) Impairment of mitochondrial respiration after cerebral hypoxia-ischemia in immature rats: relationship to activation of caspase-3 and neuronal injury. Brain Res. Dev. Brain Res. 125, 43-50.
40. Rice J. E. III, Vannucci R. C., and, Brierley J. B., (1981) The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 9, 131-141.
41. Robertson C. L., and, Saraswati M., (2015) Progesterone protects mitochondrial function in a rat model of pediatric traumatic brain injury. J. Bioenerg. Biomembr. 47, 43-51.
42. Robertson C. L., Scafidi S., McKenna M. C., and, Fiskum G., (2009) Mitochondrial mechanisms of cell death and neuroprotection in pediatric ischemic and traumatic brain injury. Exp. Neurol. 218, 371-380.
43. Rodriguez-Rodriguez A., Egea-Guerrero J. J., Murillo-Cabezas F., and, Carrillo-Vico A., (2014) Oxidative stress in traumatic brain injury. Curr. Med. Chem. 21, 1201-1211.
44. Rosenthal R. E., Williams R., Bogaert Y. E., Getson P. R., and, Fiskum G., (1992) Prevention of postischemic canine neurological injury through potentiation of brain energy metabolism by acetyl-L-carnitine. Stroke 23, 1312-1317.
45. Scafidi S., Fiskum G., Lindauer S. L., Bamford P., Shi D., Hopkins I., and, McKenna M. C., (2010a) Metabolism of acetyl-L-carnitine for energy and neurotransmitter synthesis in the immature rat brain. J. Neurochem. 114, 820-831.
46. Scafidi S., Racz J., Hazelton J., McKenna M. C., and, Fiskum G., (2010b) Neuroprotection by acetyl-L-carnitine after traumatic injury to the immature rat brain. Dev. Neurosci. 32, 480-487.
47. Sheldon R. A., Aminoff A., Lee C. L., Christen S., and, Ferriero D. M., (2007) Hypoxic preconditioning reverses protection after neonatal hypoxia-ischemia in glutathione peroxidase transgenic murine brain. Pediatr. Res. 61, 666-670.
48. Simpkins J. W., and, Singh M., (2008) More than a decade of estrogen neuroprotection. Alzheimers Dement. 4, S131-S136.
49. Singh M., Sumien N., Kyser C., and, Simpkins J. W., (2008) Estrogens and progesterone as neuroprotectants: what animal models teach us. Front Biosci. 13, 1083-1089.
50. Smith A. L., Alexander M., Rosenkrantz T. S., Sadek M. L., and, Fitch R. H., (2014) Sex differences in behavioral outcome following neonatal hypoxia ischemia: insights from a clinical meta-analysis and a rodent model of induced hypoxic ischemic brain injury. Exp. Neurol. 254, 54-67.
51. Starkov A. A., Chinopoulos C., and, Fiskum G., (2004) Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury. Cell Calcium 36, 257-264.
52. Sullivan P. G., Rippy N. A., Dorenbos K., Concepcion R. C., Agarwal A. K., and, Rho J. M., (2004) The ketogenic diet increases mitochondrial uncoupling protein levels and activity. Ann. Neurol. 55, 576-580.
53. Ten V. S., and, Starkov A., (2012) Hypoxic-ischemic injury in the developing brain: the role of reactive oxygen species originating in mitochondria. Neurol. Res. Int. 2012, 542976.
54. Ten V. S., Yao J., Ratner V., et al,. (2010) Complement component c1q mediates mitochondria-driven oxidative stress in neonatal hypoxic-ischemic brain injury. J. Neurosci. 30, 2077-2087.
55. Thornton C., Rousset C. I., Kichev A., Miyakuni Y., Vontell R., Baburamani A. A., Fleiss B., Gressens P., and, Hagberg H., (2012) Molecular mechanisms of neonatal brain injury. Neurol. Res. Int. 2012, 506320.
56. Tsuji M., Aoo N., Harada K., Sakamoto Y., Akitake Y., Irie K., Mishima K., Ikeda T., and, Fujiwara M., (2010) Sex differences in the benefits of rehabilitative training during adolescence following neonatal hypoxia-ischemia in rats. Exp. Neurol. 226, 285-292.
57. Ursini F., Maiorino M., and, Gregolin C., (1985) The selenoenzyme phospholipid hydroperoxide glutathione peroxidase. Biochim. Biophys. Acta 839, 62-70.
58. Ursini F., Maiorino M., and, Gregolin C., (1986) Phospholipid hydroperoxide glutathione peroxidase. Int. J. Tissue React. 8, 99-103.
59. Vannucci S. J., and, Hagberg H., (2004) Hypoxia-ischemia in the immature brain. J. Exp. Biol. 207, 3149-3154.
60. Waddell J., Hanscom M., Shalon E. N., McKenna M. C., and, McCarthy M. M., (2016) Sex differences in cell genesis, hippocampal volume and behavioral outcomes in a rat model of neonatal HI. Exp. Neurol. 275, 285-295.
61. Weis S. N., Pettenuzzo L. F., Krolow R., Valentim L. M., Mota C. S., Dalmaz C., Wyse A. T., and, Netto C. A., (2012) Neonatal hypoxia-ischemia induces sex-related changes in rat brain mitochondria. Mitochondrion 12, 271-279.
62. Xu S., Waddell J., Zhu W., Shi D., Marshall A. D., McKenna M. C., and, Gullapalli R. P., (2015) In vivo longitudinal proton magnetic resonance spectroscopy on neonatal hypoxic-ischemic rat brain injury: neuroprotective effects of acetyl-L-carnitine. Magn. Reson. Med. 74, 1530-1542.
63. Yang G., Chan P. H., Chen J., Carlson E., Chen S. F., Weinstein P., Epstein C. J., and, Kamii H., (1994) Human copper-zinc superoxide dismutase transgenic mice are highly resistant to reperfusion injury after focal cerebral ischemia. Stroke 25, 165-170.
64. Yant L. J., Ran Q., Rao L., Van R. H., Shibatani T., Belter J. G., Motta L., Richardson A., and, Prolla T. A., (2003) The selenoprotein GPX4 is essential for mouse development and protects from radiation and oxidative damage insults. Free Radic. Biol. Med. 34, 496-502.
65. Yoo S. E., Chen L., Na R., Liu Y., Rios C., Van R. H., Richardson A., and, Ran Q., (2012) Gpx4 ablation in adult mice results in a lethal phenotype accompanied by neuronal loss in brain. Free Radic. Biol. Med. 52, 1820-1827.
66. Zanelli S. A., Solenski N. J., Rosenthal R. E., and, Fiskum G., (2005) Mechanisms of ischemic neuroprotection by acetyl-L-carnitine. Ann. N. Y. Acad. Sci. 1053, 153-161.
67. Zheng J., and, Bizzozero O. A., (2010) Accumulation of protein carbonyls within cerebellar astrocytes in murine experimental autoimmune encephalomyelitis. J. Neurosci. Res. 88, 3376-3385.