Cerebellar axon/myelin loss, angiogenic sprouting, and neuronal increase of vascular endothelial growth factor in a preterm infant with kernicterus

Journal of Child Neurology

Volumn 27, Issue 5, 2012, Pages 615-624

  Brito, Maria A ^a   Zurolo, Emanuele ^b   Pereira, Pedro ^c,d   Barroso, Cĝndida ^c,d   Aronica, Eleonora ^b   Brites, Dora ^a  

^a RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c HOSPITAL DE SANTA MARIA   (Portugal)

^d UNIVERSITY OF LISBON   (Portugal)

Author keywords

angiogenesis; kernicterus; multidrug resistance associated protein 1; neuronal impairment; vascular endothelial growth factor

Indexed keywords

BILIRUBIN; CLONAZEPAM; FLUCLOXACILLIN; GENTAMICIN; LIDOCAINE; MIDAZOLAM; MULTIDRUG RESISTANCE PROTEIN 1; MYELIN; PENICILLIN G; PHENOBARBITAL; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

APGAR SCORE; ARTICLE; ARTIFICIAL VENTILATION; AUTOPSY; BILIRUBIN BLOOD LEVEL; BRADYCARDIA; CARDIOPULMONARY INSUFFICIENCY; CASE REPORT; CRYING; DENTATE NUCLEUS; FEMALE; GRAND MAL SEIZURE; HUMAN; HYPERBILIRUBINEMIA; HYPOTENSION; INFANT; KERNICTERUS; LUNG INFILTRATE; MALE; METABOLIC ACIDOSIS; MORTALITY; MUSCLE HYPOTONIA; NERVE CELL; NERVE FIBER; NERVE SPROUTING; NEUROTOXICITY; PHOTOTHERAPY; PNEUMONIA; PREMATURITY; PRIORITY JOURNAL; PURKINJE CELL; SEPSIS; SILVER STAINING; SUCKLING; UPREGULATION; X RAY FILM;

AXONS; CEREBELLUM; CLAUDINS; HUMANS; INFANT, NEWBORN; KERNICTERUS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MYELIN SHEATH; NEOVASCULARIZATION, PATHOLOGIC; PREMATURE BIRTH; PURKINJE CELLS; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84860299959     PISSN: 08830738     EISSN: 17088283     Source Type: Journal    
DOI: 10.1177/0883073811423975     Document Type: Article

References (46)

1. Brito MA, Silva RFM, Brites D New Trends in Brain Research. Chen FJ, ed. New York: Nova Science ; 2006: 1-38.
2. Smitherman H, Stark AR, Bhutani VK. Early recognition of neonatal hyperbilirubinemia and its emergent management. Semin Fetal Neonatal Med. 2006 ; 11 (3). 214-224
3. Shapiro SM. Chronic bilirubin encephalopathy: diagnosis and outcome. Semin Fetal Neonatal Med. 2010 ; 15 (3). 157-163
4. Bhutani VK, Johnson L. Prevention of severe neonatal hyperbilirubinemia in healthy infants of 35 or more weeks of gestation: implementation of a systems-based approach. J Pediatr (Rio J). 2007 ; 83 (4). 289-293 (Pubitemid 47328107)
5. Ebbesen F. Recurrence of kernicterus in term and near-term infants in Denmark. Acta Paediatr. 2000 ; 89 (10). 1213-1217
6. Hansen TWR. Kernicterus in term and near-term infants-the specter walks again. Acta Paediatr. 2000 ; 89 (10). 1155-1157
7. Palmer RH, Keren R, Maisels MJ, Yeargin-Allsopp M. National Institute of Child Health and Human Development (NICHD) conference on kernicterus: a population perspective on prevention of kernicterus. J Perinatol. 2004 ; 24 (11). 723-725 (Pubitemid 39504413)
8. Falcão AS, Bellarosa C, Fernandes A, et al. Role of multidrug resistance-associated protein 1 expression in the in vitro susceptibility of rat nerve cell to unconjugated bilirubin. Neuroscience. 2007 ; 144 (3). 878-888 (Pubitemid 46019843)
9. Falcão AS, Silva RFM, Pancadas S, Fernandes A, Brito MA, Brites D. Apoptosis and impairment of neurite network by short exposure of immature rat cortical neurons to unconjugated bilirubin increase with cell differentiation and are additionally enhanced by an inflammatory stimulus. J Neurosci Res. 2007 ; 85 (6). 1229-1239 (Pubitemid 46724366)
10. Brito MA, Brites D. Effect of acidosis on bilirubin-induced toxicity to human erythrocytes. Mol Cell Biochem. 2003 ; 247 (1-2). 155-162 (Pubitemid 36798520)
11. Fernandes A, Silva RFM, Falcão AS, Brito MA, Brites D. Cytokine production, glutamate release and cell death in rat cultured astrocytes treated with unconjugated bilirubin and LPS. J Neuroimmunol. 2004 ; 153 (1-2). 64-75 (Pubitemid 38950928)
12. Vaz AR, Silva SL, Barateiro A. Pro-inflammatory cytokines intensify the activation of NO/NOS, JNK1/2 and caspase cascades in immature neurons exposed to elevated levels of unconjugated bilirubin. Exp Neurol. 2011 ; 229 (2). 381-390
13. Dennery PA, Seidman DS, Stevenson DK. Neonatal hyperbilirubinemia. N Engl J Med. 2001 ; 344 (8). 581-590
14. Watchko JF, Maisels MJ. Jaundice in low birthweight infants: pathobiology and outcome. Arch Dis Child Fetal Neonatal Ed. 2003 ; 88 (6). F455 - F458 (Pubitemid 37449416)
15. Brito MA, Rosa AI, Falc , ão AS, et al. Unconjugated bilirubin differentially affects the redox status of neuronal and astroglial cells. Neurobiol Dis. 2008 ; 29 (1). 30-40 (Pubitemid 350180480)
16. Fernandes A, Falcão AS, Abranches E, et al. Bilirubin as a determinant for altered neurogenesis, neuritogenesis, and synaptogenesis. Dev Neurobiol. 2009 ; 69 (9). 568-582
17. Silva SL, Vaz AR, Barateiro A, et al. Features of bilirubin-induced reactive microglia: from phagocytosis to inflammation. Neurobiol Dis. 2010 ; 40 (3). 663-675
18. Palmela I, Cardoso FL, Bernas M, et al. Elevated levels of bilirubin and long-term exposure impair human brain microvascular endothelial cell integrity. Curr Neurovasc Res. 2011 ; 8 (2). 153-169
19. Dulak J, Łoboda A, Zagórska A, Józkowicz A. Complex role of heme oxygenase-1 in angiogenesis. Antioxid Redox Signal. 2004 ; 6 (5). 858-866 (Pubitemid 39237939)
20. Cardoso FL, Brites D, Brito MA. Looking at the blood-brain barrier: molecular anatomy and possible investigation approaches. Brain Res Rev. 2010 ; 64 (2). 328-363
21. Perlman JM, Rogers BB, Burns D. Kernicteric findings at autopsy in two sick near term infants. Pediatrics. 1997 ; 99 (4). 612-615 (Pubitemid 27176449)
22. Gkoltsiou K, Tzoufi M, Counsell S, Rutherford M, Cowan F. Serial brain MRI and ultrasound findings: relation to gestational age, bilirubin level, neonatal neurologic status and neurodevelopmental outcome in infants at risk of kernicterus. Early Hum Dev. 2008 ; 84 (12). 829-838
23. Schutta HS, Johnson L. Bilirubin encephalopathy in the Gunn rat: a fine structure study of the cerebellar cortex. J Neuropathol Exp Neurol. 1967 ; 26 (3). 377-396
24. Lin S, Wei X, Bales KR, et al. Minocycline blocks bilirubin neurotoxicity and prevents hyperbilirubinemia-induced cerebellar hypoplasia in the Gunn rat. Eur J Neurosci. 2005 ; 22 (1). 21-27 (Pubitemid 41059968)
25. Aronica E, Gorter JA, Jansen GH, et al. Expression and cellular distribution of multidrug transporter proteins in two major causes of medically intractable epilepsy: focal cortical dysplasia and glioneuronal tumors. Neuroscience. 2003 ; 118 (2). 417-429 (Pubitemid 36423257)
26. Boer K, Troost D, Jansen F, et al. Clinicopathological and immunohistochemical findings in an autopsy case of tuberous sclerosis complex. Neuropathology. 2008 ; 28 (6). 577-590
27. Bellarosa C, Bortolussi G, Tiribelli C, et al. The role of ABC transporters in protecting cells from bilirubin toxicity. Curr Pharm Des. 2009 ; 15 (25). 2884-2892
28. Wennberg RP. The blood-brain barrier and bilirubin encephalopathy. Cell Mol Neurobiol. 2000 ; 20 (1). 97-109 (Pubitemid 30090918)
29. Burgess GH, Oh W, Bratlid D. The effects of brain blood flow on brain bilirubin deposition in newborn piglets. Pediatr Res. 1985 ; 19 (7). 691-696 (Pubitemid 15006485)
30. Li J, Stuhlmann H. In vitro imaging of angiogenesis using embryonic stem cell-derived endothelial cells. Stem Cells Dev. 2011 ;:
31. Raimondi F, Crivaro V, Capasso L, et al. Unconjugated bilirubin modulates the intestinal epithelial barrier function in a human-derived in vitro model. Pediatr Res. 2006 ; 60 (1). 30-33 (Pubitemid 44297608)
32. McCall IC, Betanzos A, Weber DA, Nava P, Miller GW, Parkos CA. Effects of phenol on barrier function of a human intestinal epithelial cell line correlate with altered tight junction protein localization. Toxicol Appl Pharmacol. 2009 ; 241 (1). 61-70
33. Brito MA, Brondino CD, Moura JJG, Brites D. Effects of bilirubin molecular species on membrane dynamic properties of human erythrocyte membranes: a spin label electron paramagnetic resonance spectroscopy study. Arch Biochem Biophys. 2001 ; 387 (1). 57-65 (Pubitemid 32989025)
34. Rodrigues CMP, Solá S, Brito MA, Brites D, Moura JJG. Bilirubin directly disrupts membrane lipid polarity and fluidity, protein order, and redox status in rat mitochondria. J Hepatol. 2002 ; 36 (3). 335-341 (Pubitemid 34194792)
35. Pagès G, Pouysségur J. Transcriptional regulation of the vascular endothelial growth factor gene-a concert of activating factors. Cardiovasc Res. 2005 ; 65 (3). 564-573 (Pubitemid 40138977)
36. Brites D, Fernandes A, Falcão AS, Gordo AC, Silva RFM, Brito MA. Biological risks for neurological abnormalities associated with hyperbilirubinemia. J Perinatol. 2009 ; 29 (suppl 1). S8 - S13
37. Hachiya Y, Hayashi M. Bilirubin encephalopathy: a study of neuronal subpopulations and neurodegenerative mechanisms in 12 autopsy cases. Brain Dev. 2008 ; 30 (4). 269-278 (Pubitemid 351335327)
38. Watchko JF. Kernicterus and the molecular mechanisms of bilirubin-induced CNS injury in newborns. Neuromolecular Med. 2006 ; 8 (4). 513-529
39. Daood M, Tsai C, Ahdab-Barmada M, Watchko JF. ABC transporter (P-gp/ABCB1, MRP1/ABCC1, BCRP/ABCG2) expression in the developing human CNS. Neuropediatrics. 2008 ; 39 (4). 211-218
40. Nag S, Manias JL, Stewart DJ. Pathology and new players in the pathogenesis of brain edema. Acta Neuropathol. 2009 ; 118 (2). 197-217
41. Roscoe WA, Welsh ME, Carter DE, Karlik SJ. VEGF and angiogenesis in acute and chronic MOG((35-55)) peptide induced EAE. J Neuroimmunol. 2009 ; 209 (1-2). 6-15
42. Martich-Kriss V, Kollias SS, Ball WS. MR findings in kernicterus. AJNR Am J Neuroradiol. 1995 ; 16 (4suppl). 819-821
43. Loftspring MC, Johnson HL, Feng R, Johnson AJ, Clark JF. Unconjugated bilirubin contributes to early inflammation and edema after intracerebral hemorrhage. J Cereb Blood Flow Metab. 2011 ; 31 (4). 1133-1142
44. Corich L, Aranda A, Carrassa L, Bellarosa C, Ostrow JD, Tiribelli C. The cytotoxic effect of unconjugated bilirubin in human neuroblastoma SH-SY5Y cells is modulated by the expression level of MRP1 but not MDR1. Biochem J. 2009 ; 417 (1). 305-312
45. Gazzin S, Berengeno AL, Strazielle N. Modulation of Mrp1 (ABCc1) and Pgp (ABCb1) by bilirubin at the blood-CSF and blood-brain barriers in the Gunn rat. PLoS One. 2011 ; 6 (1). e16165
46. Conlee JW, Shapiro SM. Development of cerebellar hypoplasia in jaundiced Gunn rats: a quantitative light microscopic analysis. Acta Neuropathol. 1997 ; 93 (5). 450-460 (Pubitemid 27186985)