Neonatal hypoxic-ischemic encephalopathy reduces c-Fos activation in the rat hippocampus: Evidence of a long-lasting effect

International Journal of Developmental Neuroscience

Volumn 38, Issue , 2014, Pages 213-222

  Souza, Andressa ^a,b,d   Dussan Sarria, Jairo Alberto ^a   Medeiros, Liciane Fernandes ^a,b   Souza, Ana Cláudia ^a,b   Oliveira, Carla ^a,b   Scarabelot, Vanessa Leal ^a,b   Adachi, Lauren Naomi ^a,b   Winkelmann Duarte, Elisa Cristiana ^c   Philippi Martins, Bárbara Beatriz ^c   Netto, Carlos Alexandre ^a   Caumo, Wolnei ^a   Torres, Iraci L S ^a,b  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

^c FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^d Mestrado em Avaliacao de Impactos Ambientais em Mineracao Victor Barreto   (Brazil)

Author keywords

BDNF; C Fos protein; Neonatal hypoxia ischemia encephalopathy; Nociceptive behavior; TNF

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; LACTATE DEHYDROGENASE; PROTEIN C FOS; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL ACTIVATION; CELL COUNT; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HOT PLATE TEST; HYPOXIC ISCHEMIC ENCEPHALOPATHY; LACTATE DEHYDROGENASE BLOOD LEVEL; MALE; NERVE CELL; NERVE CELL PLASTICITY; NEWBORN; NOCICEPTION; NONHUMAN; PERINATAL PERIOD; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; TAIL FLICK TEST; VON FREY TEST;

RATTUS;

EID: 84910033345     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2014.09.003     Document Type: Article

References (76)

1. Anand K.J., Hickey P.R. Pain and its effects in the human neonate and fetus. N. Engl. J. Med. 1987, 317:1321-1329.
2. Anand K.J. Clinical importance of pain and stress in preterm neonates. Biol. Neonate 1998, 73:1-9.
3. Andrews K., Fitzgerald M. Biological barriers to paediatric pain management. Clin. J. Pain 1997, 13:138-143.
4. Anseloni V.C., He F., Novikova S.I., Turnbach Robbins M., Lidow I.A., Ennis M., Lidow M.S. Alterations in stress-associated behaviors and neurochemical markers in adult rats after neonatal short-lasting local inflammatory insult. Neuroscience 2005, 131:635-645.
5. Arteni N.S., Salgueiro J., Torres I., Achaval M., Netto C.A. Neonatal cerebral hypoxia-ischemia causes lateralized memory impairments in the adult rat. Brain Res. 2003, 973:171-178.
6. Arteni N.S., Pereira L.O., Rodrigues A.L., Lavinsky D., Achaval M.E., Netto C.A. Lateralized and sex-dependent behavioral and morphological effects of unilateral neonatal cerebral hypoxia-ischemia in the rat. Behav. Brain Res. 2010, 210:92-98.
7. Baker H., Lindsay J., Weisbroth S. The Laboratory Rat 1979, 79-82. Academic Press, New York. H. Baker, J. Linday (Eds.).
8. Bartha A.I., Shen J., Katz K.H., Mischel R.E., Yap K.R., Ivacko J.A., Andrews E.M., Ferriero D.M., Ment L.R., Silverstein F.S. Neonatal seizures: multicenter variability in current treatment practices. Pediatr. Neurol. 2007, 37:85-90.
9. Berger R., Garnier Y., Jensen A. Perinatal brain damage: underlying mechanisms and neuroprotective strategies. J. Soc. Gynecol. Investig. 2002, 9:319-328.
10. Bhutta A.T., Rovnaghi C., Simpson P.M., Gossett J.M., Scalzo F.M., Anand K.J. Interactions of inflammatory pain and morphine in infant rats. Long-term behavioral effects. Physiol. Behav. 2001, 73:51-58.
11. Boucher T., Jennings E., Fitzgerald M. The onset of diffuse noxious inhibitory controls in postnatal rat pups: a c-Fos study. Neurosci. Lett. 1998, 257:9-12.
12. Bullock R., Zauner A., Woodward J., Young H.F. Massive persistent release of excitatory amino acids following human occlusive stroke. Stroke 1995, 26:2187-2189.
13. Castilho V.M., Macedo C.E., Brandão M.L. Role of benzodiazepine and serotonergic mechanisms in conditioned freezing and antinociception using electrical stimulation of the dorsal periaqueductal gray as unconditioned stimulus in rats. Psychopharmacology (Berl) 2002, 165:77-85.
14. Deshpande J.K., Anand K. Basic aspects of acute pediatric pain and sedation. The Pediatric Pain Handbook 1996, 1-48. J.K. Deshpande, J.D. Tobias (Eds.).
15. Dobbing J., Sands J. Comparative aspects of the brain growth spurt. Early Hum. Dev. 1979, 3:79-83.
16. Dragunow M., Faull R. The use of c-Fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Methods 1989, 29:261-265.
17. Fang A.Y., Gonzalez F.F., Sheldon R.A., Ferriero D.M. Effects of combination therapy using hypothermia and erythropoietin in a rat model of neonatal hypoxia-ischemia. Pediatr. Res. 2013, 73:12-17.
18. Fitzgerald M.J. Perinatal changes in epidermal innervation in rat and mouse. J. Comp. Neurol. 1966, 126:37-41.
19. Fitzgerald M. The development of nociceptive circuits. Nat. Rev. Neurosci. 2005, 6:507-520.
20. Gilby K.L., Armstrong J.N., Currie R.W., Robertson H.A. The effects of hypoxia-ischemia on expression of c-Fos, c-Jun and Hsp70 in the young rat hippocampus. Brain Res. Mol. Brain Res. 1997, 48:87-96.
21. Gundersen H.J. Notes on the estimation on the numerical density of arbitrary profiles: the edge effect. J. Microsc. 1977, 111:219-223.
22. Guy E.R., Abbott F.V. The behavioral response to formalin in preweanling rats. Pain 1992, 51:81-90.
23. Hamrick S.E., Ferriero D.M. The injury response in the term newborn brain: can we neuroprotect?. Curr. Opin. Neurol. 2003, 16:147-154.
24. Hermansen C.L., Lorah K.N. Respiratory distress in the newborn. Am. Fam. Physician 2007, 76:987-994.
25. Hill C.A., Threlkeld S.W., Fitch R.H. Reprint of "Early testosterone modulated sex differences in behavioral outcome following neonatal hypoxia ischemia in rats". Int. J. Dev. Neurosci. 2011, 29:621-628.
26. Hohmann A.G., Neely M.H., Pina J., Nackley A.G. Neonatal chronic hind paw inflammation alters sensitization to intradermal capsaicin in adult rats: a behavioral and immunocytochemical study. J. Pain 2005, 6:798-808.
27. Jacobs S.E., Berg M., Hunt R., Tarnow-Mordi W.O., Inder T.E., Davis P.G. Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst. Rev. 2013, 1:CD003311.
28. Jensen F.E. Developmental factors regulating susceptibility to perinatal brain injury and seizures. Curr. Opin. Pediatr. 2006, 18:628-633.
29. Karlsson M., Blennow M., Nemeth A., Winbladh B. Dynamics of hepatic enzyme activity following birth asphyxia. Acta Paediatr. 2006, 95:1405-1411.
30. Karlsson M., Wiberg-Itzel E., Chakkarapani E., Blennow M., Winbladh B., Thoresen M. Lactate dehydrogenase predicts hypoxic ischaemic encephalopathy in newborn infants: a preliminary study. Acta Paediatr. 2010, 99:1139-1144.
31. Kostovic I., Rakic P. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J. Comp. Neurol. 1990, 297:441-470.
32. Lackmann G.M., Tollner U., Mader R. Serum enzyme activities in full-term asphyxiated and healthy newborns: enzyme kinetics during the first 144h of life. Enzyme Protein 1993, 47:160-172.
33. Le Bars D., Gozariu M., Cadden S.W. Animal models of nociception. Pharmacol. Rev. 2001, 53:597-652.
34. Lehner M., Taracha E., Skórzewska A., Maciejak P., Wisłowska-Stanek A., Zienowicz M., Szyndler J., Bidziński A., Płaźnik A. Behavioral, immunocytochemical and biochemical studies in rats differing in their sensitivity to pain. Behav. Brain Res. 2006, 171:189-198.
35. Levine S. Anoxic-ischemic encephalopathy in rats. Am. J. Pathol. 1960, 36:1-17.
36. Lim S.H., Lee J.S., Lee J.I., Im S., Ko Y.J., Kim H.W. The quantitative assessment of functional impairment and its correlation to infarct volume in rats with transient middle cerebral artery occlusion. Brain Res. 2008, 1230:303-309.
37. Lin C., Al-Chaer E.D. Long-termsensitization of primary afferents in adult rats exposed to neonatal colon pain. Brain Res. 2003, 971:73-82.
38. Liu T., Clark R.K., McDonnell P.C., Young P.R., White R.F., Barone F.C., Feuerstein G.Z. Tumor necrosis factor-alpha expression in ischemic neurons. Stroke 1994, 25:1481-1488.
39. Low J.A. The relationship of asphyxia in the mature fetus to long-term neurologic function. Clin. Obstet. Gynaecol. 1993, 36:82-90.
40. Marsh D.F., Hatch D.J., Fitzgerald M. Opioid system and the newborn. Br. J. Anaesth. 1997, 79:787-795.
41. Medeiros L.F. Efeito da administração de anestésicos gerais, associado ou não ao procedimento cirúrgico, sobre: parâmetros comportamentais, atividades e-ntpdásica e de ecto-5'-nucleotidase em medula espinhal de ratos 2010, (Master's thesis), Universidade Federal do Rio Grande do Sul, Graduate Program in Biological Sciences: Physiology.
42. Nakamura H., Katayama Y., Kawakami Y. Hippocampal CA1/subiculum-prefrontal cortical pathways induce plastic changes of nociceptive responses in cingulated and prelimbic areas. BMC Neurosci. 2010, 11:100.
43. Ness J.M., Harvey C.R., Washington J.D., Roth K.A., Carroll S.L., Zhang J. Differential activation of c-fos and caspase-3 in hippocampal neuron subpopulations following neonatal hypoxia-ischemia. J. Neurosci. Res. 2008, 86:1115-1124.
44. Netto C.A., Siegfried B., Izquierdo I. Analgesia induced by exposure to a novel environment in rats: effect of a concurrent and post-training stressful stimulation. Behav. Neural. Biol. 1987, 48:304-309.
45. O'Connor J.J. Targeting tumour necrosis factor-α in hypoxia and synaptic signalling. Ir. J. Med. Sci. 2013, 182:157-162.
46. Park H., Poo M.M. Neurotrophin regulation of neural circuit development and function. Nat. Rev. Neurosci. 2013, 14:7-23.
47. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2008, Academic Press, San Diego. 6th ed.
48. Ramirez M.R., Muraro F., Zylbersztejn D.S., Abel C.R., Arteni N.S., Lavinsky D., Netto C.A., Trindade V.M. Neonatal hypoxia-ischemia reduces ganglioside, phospholipid and cholesterol contents in the rat hippocampus. Neurosci. Res. 2003, 46:339-347.
49. Randich A., Uzzell T., DeBerry J.J., Ness T.J. Neonatal urinary bladder inflammation produces adult bladder hypersensitivity. J. Pain 2006, 7:469-479.
50. Rasmussen P., Brassard P., Adser H., Pedersen M.V., Leick L., Hart E., Secher N.H., Pedersen B.K., Pilegaard H. Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp. Physiol. 2009, 94:1062-1069.
51. Reichert A.P.S., Silva S.L.F., Oliveira J.M. Dor no recém-nascido: uma realidade a ser considerada. Rev. Nursing 2000, 3:28-30.
52. Ribeiro S., Yang P., Reyes-Vazquez C., Swann A., Dafny N. Sex differences in tail-flick latency of non-stressed and stressed rats. Int. J. Neurosci. 2005, 115:1383-1395.
53. Rice J.E., Vannucci R.C., Brierley J.B. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 1981, 9:131-141.
54. Ruda M.A., Ling Q.D., Hohmann A.G., Peng Y.B., Tachibana T. Altered nociceptive neuronal circuits after neonatal peripheral inflammation. Science 2000, 289:628-631.
55. Ryan S., Taylor C.T., McNicholas W.T. Predictors of elevated nuclear factor-kappaB-dependent genes in obstructive sleep apnea syndrome. Am. J. Respir. Crit. Care Med. 2006, 174:824-830.
56. Savransky V., Bevans S., Nanayakkara A., Li J., Smith P.L., Torbenson M.S., Polotsky V.Y. Chronic intermittent hypoxia causes hepatitis in a mouse model of diet-induced fatty liver. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 293:G871-G877.
57. Silveira P.P., Portella A.K., Clemente Z., Gamaro G.D., Dalmaz C. The effect of neonatal handling on adult feeding behavior is not an anxiety-like behavior. Int. J. Dev. Neurosci. 2005, 23:93-99.
58. Silveira P.P., Portella A.K., Assis S.A., Nieto F.B., Diehl L.A., Crema L.M., Peres W., Costa G., Scorza C., Quillfeldt J.A., Lucion A.B., Dalmaz C. Early life experience alters behavioral responses to sweet food and accumbal dopamine metabolism. Int. J. Dev. Neurosci. 2010, 28:111-118.
59. +-ATPase activity and the vulnerability/resilience to mood disorders induced by early life experience. Neurochem. Res. 2011, 36:2075-2082.
60. Tam C.S., Wong M., Tam K., Aouad L., Waters K.A. The effect of acute intermittent hypercapnic hypoxia treatment on IL-6, TNF-alpha, and CRP levels in piglets. Sleep 2007, 30:723-727.
61. Tanaka T. The relationships between litter size, offspring weight and behavioral development in laboratory mice. Mammal Study 2004, 29:147-153.
62. Taniguchi T., Fukunaga R., Matsuoka Y., Terai K., Tooyama I., Kimura H. Delayed expression of c-fos protein in rat hippocampus and cerebral cortex following transient in vivo exposure to hypoxia. Brain Res. 1994, 640:119-125.
63. Thoresen M., Liu X., Jary S., Brown E., Sabir H., Stone J., Cowan F., Karlsson M. Lactate dehydrogenase in hypothermia-treated newborn infants with hypoxic-ischaemic encephalopathy. Acta Paediatr. 2012, 101:1038-1044.
64. Tulchinsky E. Fos family members: regulation, structure and role in oncogenic transformation. Histol. Histopathol. 2000, 15:921-928.
65. Tuor U.I., Del Bigio M.R., Chumas P.D. Brain damage due to cerebral hypoxia/ischemia in the neonate: pathology and pharmacological modification. Cerebrovasc. Brain Metab. Rev. 1996, 8:159-193.
66. van Handel M., Swaab H., de Vries L.S., Jongmans M.J. Long-term cognitive and behavioral consequences of neonatal encephalopathy following perinatal asphyxia: a review. Eur. J. Pediatr. 2007, 166:645-654.
67. VanElzakker M., Fevurly R.D., Breindel T., Spencer R.L. Environmental novelty is associated with a selective increase in Fos expression in the output elements of the hippocampal formation and the perirhinal cortex. Learn. Mem. 2008, 15:899-908.
68. Van Praag H., Frenk H. Evidence for opiate tolerance en newborn rats. Dev. Brain Res. 1991, 60:99-102.
69. Volpe J.J. Neurobiology of periventricular leukomalacia in the premature infant. Pediatr. Res. 2001, 50:553-562.
70. Volpe J.J. Neurobiology of the Newborn 2008, Saunders Elsevier, Philadephia, PA. 5th ed.
71. Wang G., Ji Y., Lidow M.S., Traub R.J. Neonatal hind paw injury alters processing of visceral and somatic nociceptive stimuli in the adult rat. J. Pain 2004, 5:440-449.
72. Weber E.D., Stelzner D.J. Behavioral effects of spinal cord transection in the developing rat. Brain Res. 1977, 125:241-255.
73. Wei F., Xu Z., Qu Z., Milbrandt J., Zhuo M. Role of EGR1 in hippocampal synaptic enhancement induced by tetanic stimulation and amputation. J. Cell Biol. 2000, 149:1325-1334.
74. Wegert S., Ossipov M.H., Nichols M.L., Bian D., Vanderah T.W., Malan T.P., Porreca F. Differential activities of intrathecal MK-801 or morphine to alter responses to thermal and mechanical stimuli in normal or nerve-injured rats. Pain 1997, 71:57-64.
75. Winkelmann-Duarte E.C., Padilha-Hoffmann C.B., Martins D.F., Schuh A.F., Fernandes M.C., Santin R., Merlo S., Sanvitto G.L., Lucion A.B. Early-life environmental intervention may increase the number of neurons, astrocytes, and cellular proliferation in the hippocampus of rats. Exp. Brain Res. 2011, 215:163-172.
76. Zanardo V., Bondio M., Perini G., Temporin G.F. Serum glutamic-oxaloacetic transaminase and glutamic-pyruvic transaminase activity in premature and full-term asphyxiated newborns. Biol. Neonate 1985, 47:61-69.