Tyrosine phosphorylation of apoptotic proteins during hyperoxia in mitochondria of the cerebral cortex of newborn piglets

Neurochemical Research

Volumn 35, Issue 7, 2010, Pages 1003-1009

  Mudduluru, Manjula ^a   Zubrow, Alan B ^a   Ashraf, Q M ^a   Delivoria Papadopoulos, Maria ^a   Mishra, Om P ^a  

^a ST CHRISTOPHER'S HOSPITAL FOR CHILDREN   (United States)

Author keywords

Apoptosis; Bad; Bax; Bcl 2; Bcl xl; Hyperoxia; Mitochondria; Phosphorylation

Indexed keywords

PROTEIN BAD; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; TYROSINE;

ANIMAL EXPERIMENT; ARTERIAL OXYGEN TENSION; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; HYPEROXIA; MITOCHONDRION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SWINE; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; CEREBRAL CORTEX; HYPEROXIA; MITOCHONDRIA; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-BCL-2; SWINE; TYROSINE;

EID: 77953232728     PISSN: 03643190     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11064-010-0147-x     Document Type: Article

References (53)

1. B Gerstner TM DeSilva K Genz A Armstrong F Brehmer RL Neve U Felderhoff-Mueser JJ Volpe PA Rosenberg 2008 Hyperoxia causes maturation-dependent cell death in the developing white matter J Neurosci 28 1236 1245 10.1523/JNEUROSCI.3213-07.2008 1:CAS:528:DC%2BD1cXhvVSksbk%3D 18234901 (Pubitemid 351186357)
2. B Weinberger DL Laskin DE Heck JD Laskin 2002 Oxygen toxicity in premature infants Toxicol Appl Pharmacol 181 60 67 10.1006/taap.2002.9387 1:CAS:528:DC%2BD38XjvFOgtL0%3D 12030843 (Pubitemid 34615412)
3. HP Lukkarinen J Laine PO Kaapa 2003 Lung epithelial cells undergo apoptosis in neonatal respiratory distress syndrome Pediatr Res 53 254 259 1:CAS:528:DC%2BD3sXivVyntA%3D%3D 12538783
4. I Métrailler-Ruchonnet A Pagano S Carnesecchi C Ody Y Donati CB Argiroffo 2007 Bcl-2 protects against hyperoxia-induced apoptosis through inhibitionof the mitochondria-dependent pathway Free Radic Biol Med 42 1062 1074 10.1016/j.freeradbiomed.2007.01.008 17349933 (Pubitemid 46356899)
5. CR Ribeiro Carvahlo G de Paula Pinto Schettino B Maranho E Pamplona Bethlem 1998 Hyperoxia and lung diseas Curr Opm Pulm Med 4 300 304 10.1097/00063198-199809000-00010
6. MP Collins JM Lorenz JR Jetton N Paneth 2001 Hypocapnia and other ventilation-related risk factors for cerebral palsy in low birth weight infants Pediatr Res 509 712 719 10.1203/00006450-200112000-00014
7. U Felderhoff-Mueser P Bittigau M Sifringer B Jarosz E Korobowicz L Mahler T Piening A Moysich T Grune F Thor R Heumann C Bührer C Ikonomidou 2004 Oxygen causes cell death in the developing brain Neurobiol Dis 17 273 282 10.1016/j.nbd.2004.07.019 1:CAS:528:DC%2BD2cXotlSltr8%3D 15474364 (Pubitemid 39345782)
8. G Klinger J Beyene P Shah M Perlman 2005 Do hyperoxaemia and hypocapnia add to the risk of brain injury after intrapartum asphyxia? Arch Dis Child Fetal Neonatal Ed 90 F49 F52 10.1136/adc.2003.048785 1:STN:280:DC%2BD2cnjslSjtA%3D%3D 15613575 (Pubitemid 40040207)
9. R Del Maestro HH Thaw J Bjork M Planker KE Arfors 1980 Free radicals as mediators of tissue injury Acta Physiol Scand Suppl 492 43 57 6261530
10. SG Jenkinson 1993 Oxygen toxicity New Horiz 1 504 511 1:STN:280:DyaK2czntlGitA%3D%3D 8087571
11. MA Cacciuttolo L Trinh JA Lumpkin G Rao 1993 Hyperoxia induces DNA damage in mammalian cells Free Radic Biol Med 14 267 276 10.1016/0891-5849(93)90023-N 1:CAS:528:DyaK3sXitVOgsr0%3D 8458584 (Pubitemid 23066367)
12. YM Janssen B Van Houten PJ Borm BT Mossman 1993 Cell and tissue responses to oxidative damage Lab Invest 69 261 274 1:CAS:528:DyaK2cXhs1SisLs%3D 8377469
13. MA O'Reilly 2001 DNA damage and cell cycle checkpoints in hyperoxic lung injury: braking to facilitate repair Am J Physiol Lung Cell Mol Physiol 281 L291 L305 11435201
14. X Wang SW Ryter C Dai ZL Tang SC Watkins XM Yin R Song AM Choi 2003 Necrotic cell death in response to oxidant stress involves the activation of the apoptogenic caspase-8/bid pathway J Biol Chem 278 29184 29191 10.1074/jbc.M301624200 1:CAS:528:DC%2BD3sXlsl2mtr0%3D 12754217 (Pubitemid 36935834)
15. JW McDonald MV Johnston 1990 Physiological and pathophysiological roles of excitatory aminoacids during central nervous system development Brain Res Rev 15 41 70 10.1016/0165-0173(90)90011-C 2163714 (Pubitemid 20158154)
16. G Taglialatela JR Perez-Polo DK Rassin 1998 Induction of apoptosis in the CNS during development by the combination of hyperoxia and inhibition of glutathione synthesis Free Radic Biol Med 25 8 936 942 10.1016/S0891-5849(98) 00131-2 1:CAS:528:DyaK1cXnsl2isrc%3D 9840739 (Pubitemid 28538560)
17. KL King JA Cidlowski 1995 Cell cycle and apoptosis: common pathways to life and death J Cell Biochem 58 175 180 10.1002/jcb.240580206 1:CAS:528:DyaK2MXmtlOnt74%3D 7673325
18. RR Ratan TH Murphy JM Baraban 1994 Oxidative stress induces apoptosis in embryonic cortical neurons J Neurochem 62 376 379 1:CAS:528:DyaK2cXhtVeqs7g%3D 7903353
19. Z Oltvai CL Milliman SJ Korsmeyer 1993 Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death Cell 74 4 609 619 10.1016/0092-8674(93)90509-O 1:CAS:528:DyaK3sXms1eqtbs%3D 8358790 (Pubitemid 23259742)
20. MC Raff 1992 Social controls on cell survival and cell death Nature 356 397 400 10.1038/356397a0 1:STN:280:DyaK383ht1Cmtg%3D%3D 1557121
21. DT Chao SJ Korsemeyer 1998 Bcl-2 family: regulators of cell death Annu Rev Immunol 16 395 419 10.1146/annurev.immunol.16.1.395 1:CAS:528: DyaK1cXislyntLs%3D 9597135 (Pubitemid 28183370)
22. ZN Oltvai CL Milliman SJ Korsmeyer 1993 Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death Cell 74 609 619 10.1016/0092-8674(93)90509-O 1:CAS:528:DyaK3sXms1eqtbs%3D 8358790 (Pubitemid 23259742)
23. MV Lagosklonny P Giannakakou WS El-Deiry DG Kingston PI Higgs L Neckers T Fojo 1997 Raf-1/bcl-2 phosphorylation: a step from microtubule damage to cell death Cancer Res 57 130 135
24. S Haldar J Chintapalli CM Croce 1996 Taxol induces Bcl-2 phosphorylation and death of prostate cancer cells Cancer Res 56 1253 1255 1:CAS:528: DyaK28XhsFGnsbg%3D 8640809
25. ZB Hu MD Minden EA McCulloch 1998 Phosphorylation of Bcl-2 after exposure of human leukemic cells to retinoic acid Blood 92 1768 1775 1:CAS:528:DyaK1cXls1Shs7k%3D 9716607
26. EG St. Clair SJ Anderson ZN Oltvai 1997 Bcl-2 counters apoptosis by bax heterodimerization-dependent and-independent mechanisms in the T-cell lineage J Biol Chem 272 29347 29355 10.1074/jbc.272.46.29347 1:CAS:528:DyaK2sXnsVOntrg%3D 9361016 (Pubitemid 27498229)
27. T Ito X Deng B Carr WS May 1997 Bcl-2 phosphorylation required for anti-apoptosis function J Biol Chem 272 11671 11673 10.1074/jbc.272.18.11671 1:CAS:528:DyaK2sXivF2ksL0%3D 9115213 (Pubitemid 27202724)
28. Lamprechet W, Stein P, Heinz F, Weissner H (1974) Creatine phosphate. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol 4. Academic Press, New York, pp 1777-1781
29. RFG Booth TB Patel JB Clark 1980 The development of enzymes of energy metabolism in brain of a precocial (guinea pig) and noncocial (rat) species J Neurochem 43 327 366
30. NA Brutus S Hanley QM Ashraf OP Mishra M Delvoria-Papadopoulos 2009 Effect of hyperoxia on Serine phosphorylation of apoptotic proteins in mitochondrial membranes of the cerebral cortex of newborn piglets Neurochem Res 34 1219 1225 10.1007/s11064-008-9898-z 1:CAS:528:DC%2BD1MXpvFWqug%3D%3D 19169818
31. E Chang K Hornick KI Fritz OP Mishra M Delivoria-Papadopoulos 2007 Effect of hyperoxia on cortical neuronal nuclear function and programmed cell death mechanisms Neurochem Res 32 1142 1149 10.1007/s11064-007-9282-4 1:CAS:528:DC%2BD2sXlslCmtbY%3D 17401666 (Pubitemid 46817462)
32. OD Saugstad 2001 Resuscitation of the asphyxic newborn infant. New insight leads to new therapeutic possibilities Biol Neonate 79 258 260 10.1159/000047102 1:STN:280:DC%2BD3M7os1Klsw%3D%3D 11275662 (Pubitemid 32247097)
33. F Capani CF Loidl F Aguirre, et al. 2001 Changes in reactive oxygen species (ROS) production in rat brain during global perinatal asphyxia: an ESR study Brain Res 914 204 207 10.1016/S0006-8993(01)02781-0 1:CAS:528: DC%2BD3MXntV2jsLk%3D 11578613 (Pubitemid 32905447)
34. V Lievre P Becuwe A Bianchi, et al. 2001 Intracellular generation of free radicals and modifications of detoxifying enzymes in cultured neurons from the developing rat forebrain in response to transient hypoxia Neuroscience 105 287 297 10.1016/S0306-4522(01)00189-0 1:CAS:528:DC%2BD3MXlslersbY%3D 11672596 (Pubitemid 32728113)
35. AA Rosenberg E Murdaugh CW White 1989 The role of oxygen free radicals in postasphyxia cerebral hypoperfusion in newborn lambs Pediatr Res 26 215 219 10.1203/00006450-198909000-00012 1:CAS:528:DyaL1MXlvFantrk%3D 2587123
36. P Temesvari E Karg I Bodi, et al. 2001 Impaired early neurologic outcome in newborn piglets reoxygenated with 100 percent oxygen compared with room air after pneumothorax-induced asphyxia Pediatr Res 49 812 819 10.1203/00006450- 200106000-00017 1:STN:280:DC%2BD3Mzhtlyrsw%3D%3D 11385143
37. M Vento M Asensi J Sastre, et al. 2003 Oxidative stress in asphyxiated term infants resuscitated with 100% oxygen J Pediatr 142 240 246 10.1067/mpd.2003.252 1:CAS:528:DC%2BD3sXitlWgt7w%3D 12640369
38. L Frank IR Sosenko 1991 Failure of premature rabbits to increase antioxidant enzymes during hyperoxic exposure: increased susceptibility to pulmonary oxygen toxicity compared with term rabbits Pediatr Res 29 292 296 1:CAS:528:DyaK3MXktVKisbY%3D 2034478
39. G Lockitch B Jacobsen G Quigley P Dison M Pendray 1989 Selenium deficiency in low birthweight infants: an unrecognized problem J Pediatr 114 865 870 10.1016/S0022-3476(89)80154-4 1:CAS:528:DyaL1MXktVKgsrg%3D 2715900 (Pubitemid 19122990)
40. S Amin SY Chen PJ Collipp M Castro-Magana VT Maddaiah SW Klein 1980 Selenium in premature infants Nutr Metab 24 331 340 10.1159/000176279 1:CAS:528:DyaL3cXlsVymu74%3D 7192373
41. R Tubman HL Halliday D McMaster 1990 Glutathione peroxidase and selenium levels in the preterm infant Biol Neonate 58 305 310 10.1159/000243284 1:STN:280:DyaK3M7ksFCqug%3D%3D 2288992
42. F Guertin CC Roy G Lepage I Yousef B Tuchweber 1993 Liver membrane composition after short-term parenteral nutrition with and without taurine in guinea pigs Proc Soc Exp Biol Med 203 418 423 1:CAS:528:DyaK3sXmt1Gjs74%3D 8351283
43. D Van Zoeren-Grobben JH Lindeman E Houdkamp R Brand J Schrijver HM Berger 1994 Postnatal changes in plasma chain breaking antioxidants in healthy preterm infants fed formula and/or human milk Am J Clin Nutr 60 900 906 1:CAS:528:DyaK2MXivVGqsLk%3D 7985631
44. J Parker QM Ashraf W Akhter OP Mishra M Delivoria-Papadopoulos 2007 Effect of post-hypoxic reoxygenation on DNA fragmentation in cortical neuronal nuclei of newborn piglets Neurosci Lett 412 273 277 10.1016/j.neulet.2006.11.021 1:CAS:528:DC%2BD2sXnsl2mug%3D%3D 17174473 (Pubitemid 46109161)
45. L disrupts death-inducing signal complex formation in plasma membrane induced by hypoxia/reoxygenation FASEB J 18 1826 1833 10.1096/fj.04-2047com 1:CAS:528:DC%2BD2cXhtVKru7bO 15576486 (Pubitemid 39602269)
46. DM Hockenbery ZN Oltvai XM Yin CL Milliman SJ Korsmeyer 1993 Bcl-2 functions in an antioxidant pathway to prevent apoptosis Cell 75 241 251 10.1016/0092-8674(93)80066-N 1:CAS:528:DyaK3sXms1Omtr8%3D 7503812 (Pubitemid 23320288)
47. AJ Kowaltowski RG Fenton G Fiskum 2004 Bcl-2 family proteins regulate mitochondrial reactive oxygen production and protect against oxidative stress Free Radic Biol Med 37 1845 1853 10.1016/j.freeradbiomed.2004.09.005 1:CAS:528:DC%2BD2cXpsFWrsbY%3D 15528043 (Pubitemid 39441068)
48. JH Jang YJ Surh 2003 Potentiation of cellular antioxidant capacity by Bcl-2: implications for its antiapoptotic function Biochem Pharmacol 66 1371 1379 10.1016/S0006-2952(03)00487-8 1:CAS:528:DC%2BD3sXnvVeru7o%3D 14555211 (Pubitemid 38373323)
49. GR Budinger M Tso DS McClintock DA Dean JI Sznajder NS Chandel 2002 Hyperoxia-induced apoptosis does not require mitochondrial reactive oxygen species and is regulated by Bcl-2 proteins J Biol Chem 277 15654 15660 10.1074/jbc.M109317200 1:CAS:528:DC%2BD38Xjs1Wjs70%3D 11877388 (Pubitemid 34967837)
50. NS Ward AB Waxman RJ Homer LL Mantell O Einarsson Y Du JA Elias 2000 Interleukin-6-induced protection in hyperoxic acute lung injury Am J Respir Cell Mol Biol 22 535 542 1:CAS:528:DC%2BD3cXktVGisrc%3D 10783124
51. OD Saugstad 2005 Oxygen for newborns: how much is too much? J Perinatol 25 Suppl 2 S45 S49 10.1038/sj.jp.7211321 15861173 (Pubitemid 40862227)
52. R Deulofeut A Critz I Adams-Chapman A Sola 2006 Avoiding hyperoxia in infants or 1250 g is associated with improved short-and long-term outcomes J Perinatol 26 700 705 10.1038/sj.jp.7211608 1:STN:280:DC%2BD28njtFKhug%3D%3D 17036032 (Pubitemid 44650189)
53. EJ Short NK Klein BA Lewis S Fulton S Eisengart C Kercsmar J Baley LT Singer 2003 Cognitive and academic consequences of bronchopulmonary dysplasia and very low birth weight: 8-year old outcomes Pediatrics 112 359 10.1542/peds.112.5.e359