Lipopolysaccharide-induced inflammation aggravates irradiation-induced injury to the young mouse brain

Developmental Neuroscience

Volumn 35, Issue 5, 2013, Pages 406-415

  Roughton, Karolina ^a   Andreasson, Ulf ^a   Blomgren, Klas ^a,b,c   Kalm, Marie ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b QUEEN SILVIA CHILDREN'S HOSPITAL   (Sweden)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Bromodeoxyuridine; Dentate gyrus; Doublecortin; Hippocampus; Neurogenesis

Indexed keywords

INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN RADIATION; BRAIN TUMOR; DENTATE GYRUS; HIPPOCAMPUS; IMMUNOASSAY; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; RADIATION INJURY;

ANIMALS; BRAIN; CELL PROLIFERATION; CHEMOKINE CCL2; HIPPOCAMPUS; INFLAMMATION; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICROGLIA; NEUROGENESIS; NEURONS; RADIATION INJURIES;

EID: 84887432829     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000353820     Document Type: Article

References (51)

1. Saran F: Recent advances in paediatric neurooncology. Curr Opin Neurol 2002; 15: 671-677.
2. Smith MA, Seibel NL, Altekruse SF, Ries LA, Melbert DL, O'Leary M, Smith FO, Reaman GH: Outcomes for children and adolescents with cancer: challenges for the twentyfirst century. J Clin Oncol 2010; 28: 2625-2634.
3. Rosychuk RJ, Witol A, Wilson B, Stobart K: Central nervous system (CNS) tumor trends in children in a western Canadian province: a population-based 22-year retrospective study. J Neurol 2012; 259: 1131-1136.
4. Armstrong GT, Liu Q, Yasui Y, Huang S, Ness KK, Leisenring W, Hudson MM, Donaldson SS, King AA, Stovall M, Krull KR, Robison LL, Packer RJ: Long-term outcomes among adult survivors of childhood central nervous system malignancies in the childhood cancer survivor study. J Natl Cancer Inst 2009; 101: 946-958.
5. Mulhern RK, Palmer SL: Neurocognitive late effects in pediatric cancer. Curr Probl Cancer 2003; 27: 177-197.
6. Lannering B, Rosberg S, Marky I, Moell C, Albertsson-Wikland K: Reduced growth hormone secretion with maintained periodicity following cranial irradiation in children with acute lymphoblastic leukaemia. Clin Endocrinol (Oxf) 1995; 42: 153-159.
7. Lannering B, Marky I, Lundberg A, Olsson E: Long-term sequelae after pediatric brain tumors: their effect on disability and quality of life. Med Pediatr Oncol 1990; 18: 304-310.
8. Spiegler BJ, Bouffet E, Greenberg ML, Rutka JT, Mabbott DJ: Change in neurocognitive functioning after treatment with cranial radiation in childhood. J Clin Oncol 2004; 22: 706-713.
9. Monje ML, Palmer T: Radiation injury and neurogenesis. Curr Opin Neurol 2003; 16: 129-134.
10. Fukuda H, Fukuda A, Zhu C, Korhonen L, Swanpalmer J, Hertzman S, Leist M, Lannering B, Lindholm D, Bjork-Eriksson T, Marky I, Blomgren K: Irradiation-induced progenitor cell death in the developing brain is resistant to erythropoietin treatment and caspase inhibition. Cell Death Differ 2004; 11: 1166-1178.
11. Kempermann G, Jessberger S, Steiner B, Kronenberg G: Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004; 27: 447-452.
12. Fukuda A, Fukuda H, Swanpalmer J, Hertzman S, Lannering B, Marky I, Bjork-Eriksson T, Blomgren K: Age-dependent sensitivity of the developing brain to irradiation is correlated with the number and vulnerability of progenitor cells. J Neurochem 2005; 92: 569-584.
13. Monje ML, Mizumatsu S, Fike JR, Palmer TD: Irradiation induces neural precursor-cell dysfunction. Nat Med 2002; 8: 955-962.
14. Rola R, Raber J, Rizk A, Otsuka S, Vanden-Berg SR, Morhardt DR, Fike JR: Radiationinduced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp Neurol 2004; 188: 316-330.
15. Fike JR, Rosi S, Limoli CL: Neural precursor cells and central nervous system radiation sensitivity. Semin Radiat Oncol 2009; 19: 122-132.
16. Monje ML, Toda H, Palmer TD: Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003; 302: 1760-1765.
17. Kalm M, Lannering B, Bjork-Eriksson T, Blomgren K: Irradiation-induced loss of microglia in the young brain. J Neuroimmunol 2009; 206: 70-75.
18. Russo I, Barlati S, Bosetti F: Effects of neuroinflammation on the regenerative capacity of brain stem cells. J Neurochem 2011; 116: 947-956.
19. Liu M, Bing G: Lipopolysaccharide animal models for Parkinson's disease. Parkinsons Dis 2011; 2011: 327089.
20. Czeh M, Gressens P, Kaindl AM: The yin and yang of microglia. Dev Neurosci 2011; 33: 199-209.
21. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O: Inflammation is detrimental for neurogenesis in adult brain. Proc Nat Acad Sci USA 2003; 100: 13632-13637.
22. Roughton K, Kalm M, Blomgren K: Sex-dependent differences in behavior and hippocampal neurogenesis after irradiation to the young mouse brain. Eur J Neurosci 2012; 36: 2763-2772.
23. Huo K, Sun Y, Li H, Du X, Wang X, Karlsson N, Zhu C, Blomgren K: Lithium reduced neural progenitor apoptosis in the hippocampus and ameliorated functional deficits after irradiation to the immature mouse brain. Mol Cell Neurosci 2012; 51: 32-42.
24. Fowler JF: The linear-quadratic formula and progress in fractionated radiotherapy. Br J Radiol 1989; 62: 679-694.
25. Naylor AS, Bull C, Nilsson MK, Zhu C, Bjork-Eriksson T, Eriksson PS, Blomgren K, Kuhn HG: Voluntary running rescues adult hippocampal neurogenesis after irradiation of the young mouse brain. Proc Natl Acad Sci USA 2008; 105: 14632-14637.
26. Kalm M, Fukuda A, Fukuda H, Ohrfelt A, Lannering B, Bjork-Eriksson T, Blennow K, Marky I, Blomgren K: Transient inflammation in neurogenic regions after irradiation of the developing brain. Radiat Res 2009; 171: 66-76.
27. Zhu C, Gao J, Karlsson N, Li Q, Zhang Y, Huang Z, Li H, Kuhn HG, Blomgren K: Isoflurane anesthesia induced persistent, progressive memory impairment, caused a loss of neural stem cells, and reduced neurogenesis in young, but not adult, rodents. J Cereb Blood Flow Metab 2010; 30: 1017-1030.
28. Hellstrom NA, Bjork-Eriksson T, Blomgren K, Kuhn HG: Differential recovery of neural stem cells in the subventricular zone and dentate gyrus after ionizing radiation. Stem Cells 2009; 27: 634-641.
29. Bostrom M, Kalm M, Karlsson N, Hellstrom Erkenstam N, Blomgren K: Irradiation to the young mouse brain caused longterm, progressive depletion of neurogenesis but did not disrupt the neurovascular niche. J Cereb Blood Flow Metab 2013; 33: 935-943.
30. Kalm M, Karlsson N, Nilsson MK, Blomgren K: Loss of hippocampal neurogenesis, increased novelty-induced activity, decreased home cage activity, and impaired reversal learning one year after irradiation of the young mouse brain. Exp Neurol, E-pub ahead of print.
31. Georg Kuhn H, Blomgren K: Developmental dysregulation of adult neurogenesis. Eur J Neurosci 2011; 33: 1115-1122.
32. Stenzel-Poore MP, Stevens SL, King JS, Simon RP: Preconditioning reprograms the response to ischemic injury and primes the emergence of unique endogenous neuroprotective phenotypes: a speculative synthesis. Stroke 2007; 38: 680-685.
33. Lin HY, Huang CC, Chang KF: Lipopolysaccharide preconditioning reduces neuroinflammation against hypoxic ischemia and provides long-term outcome of neuroprotection in neonatal rat. Pediatr Res 2009; 66: 254-259.
34. Longhi L, Gesuete R, Perego C, Ortolano F, Sacchi N, Villa P, Stocchetti N, De Simoni MG: Long-lasting protection in brain trauma by endotoxin preconditioning. J Cereb Blood Flow Metab 2011; 31: 1919-1929.
35. Rosenzweig HL, Minami M, Lessov NS, Coste SC, Stevens SL, Henshall DC, Meller R, Simon RP, Stenzel-Poore MP: Endotoxin preconditioning protects against the cytotoxic effects of TNF? after stroke: a novel role for TNF? in LPS-ischemic tolerance. J Cereb Blood Flow Metab 2007; 27: 1663-1674.
36. Eklind S, Mallard C, Leverin AL, Gilland E, Blomgren K, Mattsby-Baltzer I, Hagberg H: Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur J Neurosci 2001; 13: 1101-1106.
37. Eklind S, Mallard C, Arvidsson P, Hagberg H: Lipopolysaccharide induces both a primary and a secondary phase of sensitization in the developing rat brain. Pediatr Res 2005; 58: 112-116.
38. Mallard C, Hagberg H: Inflammation-induced preconditioning in the immature brain. Semin Fetal Neonatal Med 2007; 12: 280-286.
39. Williamsson C, Danielsson P, Smith L: Catheter-directed foam sclerotherapy for insufficiency of the great saphenous vein: occlusion rates and patient satisfaction after one year. Phlebology, E-pub ahead of print.
40. Wang X, Rousset CI, Hagberg H, Mallard C: Lipopolysaccharide-induced inflammation and perinatal brain injury. Semin Fetal Neonatal Med 2006; 11: 343-353.
41. Nimmerjahn A, Kirchhoff F, Helmchen F: Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005; 308: 1314-1318.
42. Bulloch K, Miller MM, Gal-Toth J, Milner TA, Gottfried-Blackmore A, Waters EM, Kaunzner UW, Liu K, Lindquist R, Nussenzweig MC, Steinman RM, McEwen BS: Cd11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult, and injured mouse brain. J Comp Neurol 2008; 508: 687-710.
43. Sierra A, Encinas JM, Deudero JJ, Chancey JH, Enikolopov G, Overstreet-Wadiche LS, Tsirka SE, Maletic-Savatic M: Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 2010; 7: 483-495.
44. Ekdahl CT: Microglial activation-tuning and pruning adult neurogenesis. Front Pharmacol 2012; 3: 41.
45. Barlind A, Karlsson N, Bjork-Eriksson T, Isgaard J, Blomgren K: Decreased cytogenesis in the granule cell layer of the hippocampus and impaired place learning after irradiation of the young mouse brain evaluated using the IntelliCage platform. Exp Brain Res 2010; 201: 781-787.
46. Karlsson N, Kalm M, Nilsson MK, Mallard C, Bjork-Eriksson T, Blomgren K: Learning and activity after irradiation of the young mouse brain analyzed in adulthood using unbiased monitoring in a home cage environment. Radiat Res 2011; 175: 336-346.
47. Kalm M, Karlsson N, Nilsson MK, Blomgren K: Loss of hippocampal neurogenesis, increased motor activity and impaired reversal learning one year after irradiation of the young mouse brain. Exp Neurol, E-pub ahead of print.
48. Herx LM, Rivest S, Yong VW: Central nervous system-initiated inflammation and neurotrophism in trauma: IL-1? is required for the production of ciliary neurotrophic factor. J Immunol 2000; 165: 2232-2239.
49. Harry GJ, Kraft AD: Neuroinflammation and microglia: considerations and approaches for neurotoxicity assessment. Expert Opin Drug Metab Toxicol 2008; 4: 1265-1277.
50. Rot A, von Andrian UH: Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu Rev Immunol 2004; 22: 891-928.
51. Ransohoff RM: Chemokines and chemokine receptors: standing at the crossroads of immunobiology and neurobiology. Immunity 2009; 31: 711-721.