Neonatal anoxia in rats: Hippocampal cellular and subcellular changes related to cell death and spatial memory

Neuroscience

Volumn 284, Issue , 2015, Pages 247-259

  Takada, S H ^a,b   dos Santos Haemmerle, C A ^a   Motta Teixeira, L C ^a   Machado Nils, A V ^a   Lee, V Y ^a   Takase, L F ^c   Cruz Rizzolo, R J ^d   Kihara, A H ^b   Xavier, G F ^a   Watanabe, I S ^a   Nogueira, M I ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSIDADE FEDERAL DO ABC   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO CARLOS   (Brazil)

^d SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Apoptosis; Asphyxia; Hippocampal cell death; Neonatal hypoxia; Spatial memory; Transmission electron microscopy

Indexed keywords

CASPASE 3; CASP3 PROTEIN, RAT;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BRAIN NERVE CELL; CELL ULTRASTRUCTURE; CHROMATIN CONDENSATION; CONTROLLED STUDY; DENTATE GYRUS; DNA FRAGMENTATION; ENZYME ACTIVATION; EXCITOTOXICITY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; IMMUNOHISTOCHEMISTRY; MALE; MORRIS WATER MAZE TEST; NERVE CELL NECROSIS; NEWBORN; NEWBORN HYPOXIA; NICK END LABELING; NONHUMAN; PROTEIN CLEAVAGE; RAT; REFERENCE MEMORY; SPATIAL MEMORY; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; ANOXIA; CELL DEATH; DISEASE MODEL; HIPPOCAMPUS; MAZE TEST; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; ANOXIA; ASPHYXIA NEONATORUM; CASPASE 3; CELL DEATH; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; MALE; MAZE LEARNING; RATS, WISTAR; SPATIAL MEMORY;

EID: 84908431399     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.08.054     Document Type: Article

References (53)

1. Banasiak K.J., Haddad G.G. Hypoxia-induced apoptosis: effect of hypoxic severity and role of p53 in neuronal cell death. Brain Res 1998, 797:295-304.
2. Barrett R.D., Bennet L., Davidson J., Dean J.M., George S., Emerald B.S., Gunn A.J. Destruction and reconstruction: hypoxia and the developing brain. Birth Defects Res C Embryo Today 2007, 81:163-176.
3. Buwalda B., Nyakas C., Vosselman H.J., Luiten P.G. Effects of early postnatal anoxia on adult learning and emotion in rats. Behav Brain Res 1995, 67:85-90.
4. Cannon T.D., van Erp T.G., Rosso I.M., Huttunen M., Lonnqvist J., Pirkola T., Salonen O., Valanne L., Poutanen V.P., Standertskjold-Nordenstam C.G. Fetal hypoxia and structural brain abnormalities in schizophrenic patients, their siblings, and controls. Arch Gen Psychiatry 2002, 59:35-41.
5. Caputa M., Rogalska J., Wentowska K., Nowakowska A. Perinatal asphyxia, hyperthermia and hyperferremia as factors inducing behavioural disturbances in adulthood: a rat model. Behav Brain Res 2005, 163:246-256.
6. Carloni S., Carnevali A., Cimino M., Balduini W. Extended role of necrotic cell death after hypoxia-ischemia-induced neurodegeneration in the neonatal rat. Neurobiol Dis 2007, 27:354-361.
7. Daval J.L., Vert P. Apoptosis and neurogenesis after transient hypoxia in the developing rat brain. Semin Perinatol 2004, 28:257-263.
8. Dell'Anna E., Chen Y., Engidawork E., Andersson K., Lubec G., Luthman J., Herrera-Marschitz M. Delayed neuronal death following perinatal asphyxia in rat. Exp Brain Res 1997, 115:105-115.
9. Engidawork E., Chen Y., Dell'Anna E., Goiny M., Lubec G., Ungerstedt U., Andersson K., Herrera-Marschitz M. Effect of perinatal asphyxia on systemic and intracerebral pH and glycolysis metabolism in the rat. Exp Neurol 1997, 145:390-396.
10. Eskelinen E.L., Reggiori F., Baba M., Kovacs A.L., Seglen P.O. Seeing is believing: the impact of electron microscopy on autophagy research. Autophagy 2011, 7:935-956.
11. Galeano P., Blanco Calvo E., Madureira de Oliveira D., Cuenya L., Kamenetzky G.V., Mustaca A.E., Barreto G.E., Giraldez-Alvarez L.D., Milei J., Capani F. Long-lasting effects of perinatal asphyxia on exploration, memory and incentive downshift. Int J Dev Neurosci 2011, 29:609-619.
12. Galluzzi L., Kepp O., Kroemer G. Mitochondria: master regulators of danger signalling. Nat Rev Mol Cell Biol 2012, 13:780-788.
13. Grimaldi M., Romer I., de Apodaca M.T., Iturbe L., Catania I.D., Gonzalez J., Kolliker-Fres R., Barreto G., Capani F. Early changes in the synapses of the neostriatum induced by perinatal asphyxia. Nutr Neurosci 2012, 15:103-110.
14. Hoeger H., Engelmann M., Bernert G., Seidl R., Bubna-Littitz H., Mosgoeller W., Lubec B., Lubec G. Long term neurological and behavioral effects of graded perinatal asphyxia in the rat. Life Sci 2000, 66:947-962.
15. Jabes A., Lavenex P.B., Amaral D.G., Lavenex P. Postnatal development of the hippocampal formation: a stereological study in macaque monkeys. J Comp Neurol 2011, 519:1051-1070.
16. Johnston M.V. Excitotoxicity in neonatal hypoxia. Ment Retard Dev Disabil Res Rev 2001, 7:229-234.
17. Kirino T. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res 1982, 239:57-69.
18. Kirino T. Delayed neuronal death. Neuropathology 2000, 20(suppl.):S95-S97.
19. Kurinczuk J.J., White-Koning M., Badawi N. Epidemiology of neonatal encephalopathy and hypoxic-ischaemic encephalopathy. Early Hum Dev 2010, 86:329-338.
20. Lamkanfi M., Festjens N., Declercq W., Vanden Berghe T., Vandenabeele P. Caspases in cell survival, proliferation and differentiation. Cell Death Differ 2007, 14:44-55.
21. Leuner B., Gould E., Shors T.J. Is there a link between adult neurogenesis and learning?. Hippocampus 2006, 16:216-224.
22. Liu J.P., Chang L.R., Gao X.L., Wu Y. Different expression of caspase-3 in rat hippocampal subregions during postnatal development. Microsc Res Tech 2008, 71:633-638.
23. Lutz P.L., Prentice H.M. Sensing and responding to hypoxia, molecular and physiological mechanisms. Integr Comp Biol 2002, 42:463-468.
24. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
25. Nakajima W., Ishida A., Lange M.S., Gabrielson K.L., Wilson M.A., Martin L.J., Blue M.E., Johnston M.V. Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat. J Neurosci 2000, 20:7994-8004.
26. Nakajima W., Ishida A., Takada G. Anoxic and hypoxic immature rat model for measurement of monoamine using in vivo microdialysis. Brain Res Brain Res Protoc 1999, 3:252-256.
27. Northington F.J., Chavez-Valdez R., Martin L.J. Neuronal cell death in neonatal hypoxia-ischemia. Ann Neurol 2011, 69:743-758.
28. Northington F.J., Zelaya M.E., O'Riordan D.P., Blomgren K., Flock D.L., Hagberg H., Ferriero D.M., Martin L.J. Failure to complete apoptosis following neonatal hypoxia-ischemia manifests as "continuum" phenotype of cell death and occurs with multiple manifestations of mitochondrial dysfunction in rodent forebrain. Neuroscience 2007, 149:822-833.
29. Orrenius S., Zhivotovsky B., Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 2003, 4:552-565.
30. Petito C.K., Feldmann E., Pulsinelli W.A., Plum F. Delayed hippocampal damage in humans following cardiorespiratory arrest. Neurology 1987, 37:1281-1286.
31. Pimentel V.C., Pinheiro F.V., Kaefer M., Moresco R.N., Moretto M.B. Assessment of uric acid and lipid peroxidation in serum and urine after hypoxia-ischemia neonatal in rats. Neurol Sci 2011, 32:59-65.
32. Portera-Cailliau C., Price D.L., Martin L.J. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J Comp Neurol 1997, 378:70-87.
33. Puyal J., Ginet V., Clarke P.G. Multiple interacting cell death mechanisms in the mediation of excitotoxicity and ischemic brain damage: a challenge for neuroprotection. Prog Neurobiol 2013, 105:24-48.
34. Rogalska J., Danielisova V., Caputa M. Effect of neonatal body temperature on postanoxic, potentially neurotoxic iron accumulation in the rat brain. Neurosci Lett 2006, 393:249-254.
35. Schmued L.C., Hopkins K.J. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 2000, 874:123-130.
36. Semple B.D., Blomgren K., Gimlin K., Ferriero D.M., Noble-Haeusslein L.J. Brain development in rodents and humans: identifying benchmarks of maturation and vulnerability to injury across species. Prog Neurobiol 2013, 106-107:1-16.
37. Sheldon R.A., Hall J.J., Noble L.J., Ferriero D.M. Delayed cell death in neonatal mouse hippocampus from hypoxia-ischemia is neither apoptotic nor necrotic. Neurosci Lett 2001, 304:165-168.
38. Shors T.J., Seib T.B., Levine S., Thompson R.F. Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 1989, 244:224-226.
39. Snigdha S., Smith E.D., Prieto G.A., Cotman C.W. Caspase-3 activation as a bifurcation point between plasticity and cell death. Neurosci Bull 2012, 28:14-24.
40. Stigger F., Lovatel G., Marques M., Bertoldi K., Moyses F., Elsner V., Siqueira I.R., Achaval M., Marcuzzo S. Inflammatory response and oxidative stress in developing rat brain and its consequences on motor behavior following maternal administration of LPS and perinatal anoxia. Int J Dev Neurosci 2013, 31:820-827.
41. Suguihara C., Lessa A.C. Strategies to minimize lung injury in extremely low birth weight infants. J Pediatr (Rio J) 2005, 81:S69-S78.
42. Takada S.H., Sampaio C.A., Allemandi W., Ito P.H., Takase L.F., Nogueira M.I. A modified rat model of neonatal anoxia: development and evaluation by pulse oximetry, arterial gasometry and Fos immunoreactivity. J Neurosci Methods 2011, 198:62-69.
43. Towfighi J., Mauger D. Temporal evolution of neuronal changes in cerebral hypoxia-ischemia in developing rats: a quantitative light microscopic study. Brain Res Dev Brain Res 1998, 109:169-177.
44. Uchiyama Y., Koike M., Shibata M. Autophagic neuron death in neonatal brain ischemia/hypoxia. Autophagy 2008, 4:404-408.
45. Vannucci R.C., Connor J.R., Mauger D.T., Palmer C., Smith M.B., Towfighi J., Vannucci S.J. Rat model of perinatal hypoxic-ischemic brain damage. J Neurosci Res 1999, 55:158-163.
46. Vexler Z.S., Ferriero D.M. Molecular and biochemical mechanisms of perinatal brain injury. Semin Neonatol 2001, 6:99-108.
47. Watanabe I., Yamada E. The fine structure of lamellated nerve endings found in the rat gingiva. Arch Histol Jpn 1983, 46:173-182.
48. Watanabe I.S., Dias F.J., Mardegan Issa J.P., dos Santos Haemmerle C.A., Cury D.P., Takada S.H., Sosthenes M.C., Pereira da Silva M.C., Campos L.M., Nogueira M.I., Iyomasa M.M. Immunohistochemistry and ultrastructural characteristics of nerve endings in the oral mucosa of rat. Microscopy (Oxf) 2013, 62:259-270.
49. West M.J., Gundersen H.J. Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 1990, 296:1-22.
50. Winocur G., Wojtowicz J.M., Sekeres M., Snyder J.S., Wang S. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 2006, 16:296-304.
51. Xavier G.F., Oliveira-Filho F.J., Santos A.M. Dentate gyrus-selective colchicine lesion and disruption of performance in spatial tasks: difficulties in "place strategy" because of a lack of flexibility in the use of environmental cues?. Hippocampus 1999, 9:668-681.
52. Yang T., Zhuang L., Terrando N., Wu X., Jonhson M.R., Maze M., Ma D. A clinically relevant model of perinatal global ischemic brain damage in rats. Brain Res 2011, 1383:317-323.
53. Zhao Y.D., Ou S., Cheng S.Y., Xiao Z., He W.J., Zhang J.H., Ruan H.Z. Dendritic development of hippocampal CA1 pyramidal cells in a neonatal hypoxia-ischemia injury model. J Neurosci Res 2013, 91:1165-1173.