Exposure of foetal neural progenitor cells to IL-1β impairs their proliferation and alters their differentiation - A role for maternal inflammation?

Journal of Neurochemistry

Volumn 120, Issue 6, 2012, Pages 964-973

  Crampton, Sean J ^a   Collins, Louise M ^a   Toulouse, Andre ^a   Nolan, Yvonne M ^a   O'Keeffe, Gerard W ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Development; Inflammation; Interleukin 1 ; Neural progenitor cells; Pregnancy

Indexed keywords

CASPASE 3; INTERLEUKIN 1BETA; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NESTIN; POLY(ADENOSINE DIPHOSPHATE RIBOSE); TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL DIFFERENTIATION; CELL FATE; CELL PROLIFERATION; CONTROLLED STUDY; IMMUNE SYSTEM; IMMUNOCYTOCHEMISTRY; INFLAMMATION; MATERNAL INFLAMMATION; MESENCEPHALON; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; WESTERN BLOTTING;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTERLEUKIN-18 RECEPTOR ALPHA SUBUNIT; INTERLEUKIN-1BETA; MESENCEPHALON; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; RATS; RECEPTORS, INTERLEUKIN-1; RNA, MESSENGER; SIGNAL TRANSDUCTION; TETRAZOLIUM SALTS; THIAZOLES; TIME FACTORS;

EID: 84857915352     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07634.x     Document Type: Article

References (41)

1. Aaltonen R., Heikkinen T., Hakala K., Laine K. and Alanen A. (2005) Transfer of proinflammatory cytokines across term placenta. Obstet. Gynecol. 106, 802.
2. Ajmone Cat M. A., Cacci E., Ragazzoni Y., Minghetti L. and Biagioni S. (2010) Pro gliogenic effect of IL 1 in the differentiation of embryonic neural precursor cells in vitro. J. Neurochem. 113, 1060-1072.
3. Bell M. J. and Hallenbeck J. M. (2002) Effects of intrauterine inflammation on developing rat brain. J. Neurosci. Res. 70, 570-579. (Pubitemid 35253527)
4. Boksa P. (2010) Effects of prenatal infection on brain development and behavior: A review of findings from animal models. Brain Behav. Immun. 24, 881-897.
5. Cai Z., Pan Z.-L., Pang Y., Evans O. B. and Rhodes P. G. (2000) Cytokine Induction in Fetal Rat Brains and Brain Injury in Neonatal Rats after Maternal Lipopolysaccharide Administration. Pediatr. Res. 47, 64.
6. Cuenda A., Rouse J., Doza Y. N., Meier R., Cohen P., Gallagher T. F., Young P. R. and Lee J. C. (1995) SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 364, 229-233.
7. Depino A. M., Earl C., Kaczmarczyk E., Ferrari C., Besedovsky H., Del Rey A., Pitossi F. J. and Oertel W. H. (2003) Microglial activation with atypical proinflammatory cytokine expression in a rat model of Parkinson's disease. Eur. J. Neurosci. 18, 2731-2742. (Pubitemid 37542126)
8. Friedman W. (2001) Cytokines regulate expression of the type 1 interleukin-1 receptor in rat hippocampal neurons and glia. Exp. Neurol. 168, 23-31.
9. Gabay C., Lamacchia C. and Palmer G. (2010) IL-1 pathways in inflammation and human diseases. Nat. Rev. Rheumatol. 6, 232-241.
10. Giulian D., Young D. G., Woodward J., Brown D. C. and Lachman L. (1988) Interleukin-1 is an astroglial growth factor in the developing brain. The Journal of Neuroscience 8, 709.
11. Godoy M. C. P., Tarelli R., Ferrari C. C., Sarchi M. I. and Pitossi F. J. (2008) Central and systemic IL-1 exacerbates neurodegeneration and motor symptoms in a model of Parkinson's disease. Brain 131, 1880.
12. Huleihel M., Golan H. and Hallak M. (2004) Intrauterine infection/inflammation during pregnancy and offspring brain damages: possible mechanisms involved. Reproductive Biology and Endocrinology 2, 17.
13. Ideguchi M., Shinoyama M., Gomi M., Hayashi H., Hashimoto N. and Takahashi J. (2008) Immune or inflammatory response by the host brain suppresses neuronal differentiation of transplanted ES cell-derived neural precursor cells. J. Neurosci. Res. 86, 1936-1943.
14. Jiao J. and Chen D. F. (2008) Induction of Neurogenesis in Nonconventional Neurogenic Regions of the Adult Central Nervous System by Niche Astrocyte Produced Signals. Stem Cells 26, 1221-1230.
15. Keohane A., Ryan S., Maloney E., Sullivan A. M. and Nolan Y. M. (2010) Tumour necrosis factor-[alpha] impairs neuronal differentiation but not proliferation of hippocampal neural precursor cells: Role of Hes1. Molecular and Cellular Neuroscience 43, 127-135.
16. Koo J. W. and Duman R. S. (2008) IL-1β is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Nat. Acad. Sci. 105, 751-756.
17. Kuzumaki N., Ikegami D., Imai S. et al. (2010) Enhanced IL-1β production in response to the activation of hippocampal glial cells impairs neurogenesis in aged mice. Synapse 64, 721-728.
18. Lie D. C., Dziewczapolski G., Willhoite A. R., Kaspar B. K., Shults C. W. and Gage F. H. (2002) The adult substantia nigra contains progenitor cells with neurogenic potential. The Journal of Neuroscience 22, 6639.
19. Ling Z., Chang Q. A., Tong C. W., Leurgans S. E., Lipton J. W. and Carvey P. M. (2004) Rotenone potentiates dopamine neuron loss in animals exposed to lipopolysaccharide prenatally. Exp. Neurol. 190, 373-383. (Pubitemid 39504993)
20. Long-Smith C. M., Collins L., Toulouse A., Sullivan A. M. and Nolan Y. M. (2010) Interleukin-1 [beta] contributes to dopaminergic neuronal death induced by lipopolysaccharide-stimulated rat glia in vitro. J. Neuroimmunol. 226, 20-26.
21. McGeer P. L., Itagaki S., Boyes B. E. and McGeer E. G. (1988) Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 38, 1285-1291.
22. Meyer U., Engler A., Weber L., Schedlowski M. and Feldon J. (2008) Preliminary evidence for a modulation of fetal dopaminergic development by maternal immune activation during pregnancy. Neuroscience 154, 701-709.
23. Mirza B., Krook H., Andersson P., Larsson L. C., Korsgren O. and Widner H. (2004) Intracerebral cytokine profiles in adult rats grafted with neural tissue of different immunological disparity. Brain Res. Bull. 63, 105-118. (Pubitemid 38591392)
24. Mogi M., Harada M., Riederer P., Narabayashi H., Fujita K. and Nagatsu T. (1994a) Tumor necrosis factor-[alpha](TNF-[alpha]) increases both in the brain and in the cerebrospinal fluid from parkinsonian patients. Neurosci. Lett. 165, 208-210.
25. Mogi M., Harada M., Kondo T., Riederer P., Inagaki H., Minami M. and Nagatsu T. (1994b) Interleukin-1 [beta], interleukin-6, epidermal growth factor and transforming growth factor-[alpha] are elevated in the brain from parkinsonian patients. Neurosci. Lett. 180, 147-150.
26. Nakanishi M., Niidome T., Matsuda S., Akaike A., Kihara T. and Sugimoto H. (2007) Microglia derived interleukin 6 and leukaemia inhibitory factor promote astrocytic differentiation of neural stem/ progenitor cells. Eur. J. Neurosci. 25, 649-658.
27. Nelson K. B. and Willoughby R. E. (2000) Infection, inflammation and the risk of cerebral palsy. Curr. Opin. Neurol. 13, 133-139.
28. Nolan A. M., Nolan Y. M. and O'Keeffe G. W. (2011) IL-1 [beta] inhibits axonal growth of developing sympathetic neurons. Molecular and Cellular Neuroscience 48, 142-150.
29. O'Keeffe G. W. and Sullivan A. M. (2005) Donor age affects the differentiation of rat ventral mesencephalic stem cells. Neurosci. Lett. 375, 101-106.
30. O'Keeffe G. W., Gutierrez H., Pandolfi P. P., Riccardi C. and Davies A. M. (2008) NGF-promoted axon growth and target innervation requires GITRL-GITR signaling. Nat. Neurosci 11, 135-142. (Pubitemid 351170494)
31. Sabolek M., Baumann B., Heinrich M., Meyer A. K., Herborg A., Liebau S., Maisel M., Hermann A., Ventz K. and Schwarz J. (2009) Initiation of Dopaminergic Differentiation of Nurr1- Mesencephalic Precursor Cells Depends on Activation of Multiple Mitogen Activated Protein Kinase Pathways. Stem Cells 27, 2009-2021.
32. Snyder-Keller A. and Stark P. F. (2008) Prenatal inflammatory effects on nigrostriatal development in organotypic cultures. Brain Res. 1233, 160-167.
33. Stolp H. B. and Dziegielewska K. M. (2009) Review: Role of developmental inflammation and blood-brain barrier dysfunction in neurodevelopmental and neurodegenerative diseases. Neuropathol. Appl. Neurobiol. 35, 132-146.
34. Urakubo A., Jarskog L. F., Lieberman J. A. and Gilmore J. H. (2001) Prenatal exposure to maternal infection alters cytokine expression in the placenta, amniotic fluid, and fetal brain. Schizophr. Res. 47, 27-36. (Pubitemid 32121768)
35. Vela J. M., Molina-Holgado E., Arévalo-Martíaposn Á ., Almazán G. and Guaza C. (2002) Interleukin-1 Regulates Proliferation and Differentiation of Oligodendrocyte Progenitor Cells. Molecular and Cellular Neuroscience. 20, 489-502. (Pubitemid 34971563)
36. Vitkovic L., Bockaert J. and Jacque C. (2000) "Inflammatory" Cytokines. J. Neurochem. 74, 457-471.
37. Wagner E. F. and Nebreda A. R. (2009) Signal integration by JNK and p38 MAPK pathways in cancer development. Nat. Rev. Cancer. 9, 537-549.
38. Wang X., Fu S., Wang Y., Yu P., Hu J., Gu W., Xu X. M. and Lu P. (2007) Interleukin-1 [beta] mediates proliferation and differentiation of multipotent neural precursor cells through the activation of SAPK/JNK pathway. Molecular and Cellular Neuroscience 36, 343-354. (Pubitemid 47633199)
39. Whitney N. P., Eidem T. M., Peng H., Huang Y. and Zheng J. C. (2009) Inflammation mediates varying effects in neurogenesis: relevance to the pathogenesis of brain injury and neurodegenerative disorders. J. Neurochem. 108, 1343-1359.
40. Zaretsky M. V., Alexander J. M., Byrd W. and Bawdon R. E. (2004) Transfer of Inflammatory Cytokines Across the Placenta. Obstet. Gynecol. 103, 546-550. (Pubitemid 40459072)
41. Zhao M., Momma S., Delfani K., Carlén M., Cassidy R. M., Johansson C. B., Brismar H., Shupliakov O., Frisén J. and Janson A. M. (2003) Evidence for neurogenesis in the adult mammalian substantia nigra. Proc. Natl Acad. Sci. USA 100, 7925.