Mapping the areas sensitive to long-term endotoxin tolerance in the rat brain: A c-fos mRNA study

Journal of Neurochemistry

Volumn 93, Issue 5, 2005, Pages 1177-1188

  Vallès, Astrid ^a   Martí, Octavi ^a   Armario, Antonio ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Central amygdala; Immediate early genes; Lipopolysaccharide; Long term effects; Paraventricular hypothalamic nucleus; Stress

Indexed keywords

ENDOTOXIN; MESSENGER RNA;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; BRAIN MAPPING; BRAIN REGION; CONTROLLED STUDY; GENE INDUCTION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LOCUS CERULEUS; MALE; NEUROTOXICITY; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL; RAT; STRIA TERMINALIS;

ANIMALS; BRAIN; BRAIN MAPPING; DRUG ADMINISTRATION SCHEDULE; DRUG TOLERANCE; ENDOTOXINS; INJECTIONS; LIPOPOLYSACCHARIDES; MALE; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; TIME FACTORS; TISSUE DISTRIBUTION;

ANIMALIA;

EID: 20144372226     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03100.x     Document Type: Article

References (63)

1. Alheid G., de Omos J. S. and Beltramino C. A. (1995) Amygdala and extended amygdala, in The Rat Nervous System, 2nd edn. (Paxinos, G., ed.), pp. 495-578. Academic Press, Sydney.
2. Aston-Jones G., Shipley M. T. and Grzanna R. (1995) The locus coeruleus, A5 and A7 noradrenergic cell groups, in The Rat Nervous System (Paxinos, G., ed.), pp. 183-213. Academic Press, Sydney.
3. Belda X., Márquez C. and Armario A. (2004) Long-term effects of a single exposure to stress in adult rats on behavior and hypothalamic-pituitary- adrenal responsiveness: comparison of two outbred rat strains. Behav. Brain Res. 154, 399-408.
4. van Bockstaele E. J., Bajic D., Proudfit H. and Valentine R. J. (2001) Topographic architecture of stress-related pathways targeting the noradrenergic locus coeruleus. Physiol. Behav. 73, 273-283.
5. Bonaz B. and Rivest S. (1998) Effect of a chronic stress on CRF neuronal activity and expression of its type 1 receptor in the rat brain. Am. J. Physiol. 275, R1438-R1449.
6. Cedarbaum J. M. and Aghajanian G. K. (1978) Afferent projections to the rat locus coeruleus as determined by a retrograde tracing technique. J. Comp. Neurol. 178, 1-16.
7. Chen X. and Herbert J. (1995) Regional changes in c-fos expression in the basal forebrain and brainstem during adaptation to repeated stress: correlations with cardiovascular, hypothermic and endocrine responses. Neuroscience 64, 675-685.
8. Dal-Zotto S., Marti O. and Armario A. (2003) Glucocorticoids are involved in the long-term effects of a single immobilization stress on the hypothalamic-pituitary-adrenal axis. Psychoneuroendocrinology 28, 992-1009.
9. Derijk R., Van Rooijen N., Tilders F. J. H., Besedovsky H. O., Del Rey A. and Berkenbosch F. (1991) Selective depletion of macrophages prevents pituitary-adrenal activation in response to subpyrogenic, but not to pyrogenic, doses of bacterial endotoxin in rats. Endocrinology 128, 330-338.
10. Elenkov I. J., Kovacs K., Kiss J., Bertok L. and Vizi E. S. (1992) Lipopolysaccharide is able to bypass corticotropin-releasing factor in affecting plasma ACTH and corticosterone levels: evidence from rats with lesions in the paraventricular nucleus. J. Endocrinol. 133, 231-236.
11. Elmquist J. K. and Saper C. B. (1996) Activation of neurons projecting to the paraventricular hypothalamic nucleus by intravenous lipopolysaccharide. J. Comp. Neurol. 374, 315-331.
12. Elmquist J. K., Ackermann M. R., Register K. B., Rimler R. B., Ross L. R. and Jacobson C. D. (1993) Induction of Fos-like immunoreactivity in the rat brain following Pasteurella multocida endotoxin administration. Endocrinology 133, 3054-3057.
13. Elmquist J. K., Scammell T. E., Jacobson C. D. and Saper C. B. (1996) Distribution of Fos-like immunoreactivity in the rat brain following intravenous lipopolysaccharide administration. J. Comp. Neurol. 371, 85-103.
14. Greisman S. E. and Hornick R. B. (1976) Endotoxin tolerance, in The Role of Immunological Factors in Infectious, Allergic, and Autoimmune Processes (Beers, R. F. Jr and Bassett, E. G., eds), pp. 43-50. Raven Press, New York.
15. Hare A. S., Clarke G. and Tolchard S. (1995) Bacterial lipopolysaccharide-induced changes in Fos protein expression in the rat brain: correlation with thermoregulatory changes and plasma corticosterone. J. Neuroendocrinol. 7, 791-799.
16. Hayley S., Brebner K., Lacosta S., Merali Z. and Anisman H. (1999) Sensitization to the effects of tumor necrosis factor-α: neuroendocrine, central monoamine, and behavioral variations. J. Neurosci. 19, 5654-5665.
17. Hayley S., Staines W., Merali Z. and Anisman H. (2001a) Time-dependent sensitization of corticotropin-releasing hormone, arginine vasopressin and c-fos immunoreactivity within the mouse brain in response to tumor necrosis factor-α. Neuroscience 106, 137-148.
18. Hayley S., Lacosta S., Merali Z., van Rooijen N. and Anisman H. (2001b) Central monoamine and plasma corticosterone changes induced by a bacterial endotoxin: sensitization and cross-sensitization effects. Eur. J. Neurosci. 13, 1155-1165.
19. Hayley S., Wall P. and Anisman H. (2002) Sensitization to the neuroendocrine, central monoamine and behavioural effects of murine tumor necrosis factor-α: peripheral and central mechanisms. Eur. J. Neurosci. 15, 1061-1076.
20. Herkenham M., Lee H. Y. and Baker R. A. (1998) Temporal and spatial patterns of c-fos mRNA induced by intravenous interleukin-1: a cascade of non-neuronal cellular activation at the blood-brain barrier. J. Comp. Neurol. 400, 175-196.
21. Hofftman G. E. and Lyo D. (2002) Anatomical markers of activity in neuroendocrine systems: are we all 'fos-ed out'? J. Neuroendocrinol. 14, 259-268.
22. Kovács K. J. (1998) c-Fos as a trancription factor: a stressful (re) view from a functional map. Neurochem. Int. 33, 287-297.
23. Lacroix S., Feinstein D. and Rivest S. (1998) The bacterial endotoxin lipopolysaccharide has the ability to target the brain in upregulating its membrane CD14 receptor within specific cellular populations. Brain Pathol. 8, 625-640.
24. Laflamme N. and Rivest S. (2001) Toll-like receptor 4: the missing link of the cerebral innate immune response triggered by circulating gram-negative bacterial cell wall components. FASEB J. 15, 155-163.
25. Laflamme N., Lacroix S. and Rivest S. (1999a) An essential role of interleukin-1β in mediating NF-κB activity and COX-2 transcription in cells of the blood-brain barrier in response to a systemic and localized inflammation but not during endotoxemia. J. Neurosci. 19, 10 923-10 930.
26. Laflamme N., Feuvrier E., Richard D. and Rivest S. (1999b) Involvement of serotonergic pathways in mediating the neuronal activity and genetic transcription of neuroendocrine corticotropin-releasing factor in the brain of systemically endotoxin-challenged rats. Neuroscience 88, 223-240.
27. Laflamme N., Soucy G. and Rivest S. (2001) Circulating cell wall components derived from gram-negative, not gram-positive, bacteria cause a profound induction of the gene-encoding Toll-like receptor 2 in the CNS. J. Neurochem. 79, 648-657.
28. LeDoux J. E. (2000) Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155-184.
29. Lee S., Barbanel G. and Rivier C. (1995) Systemic endotoxin increases steady-state gene expression of hypothalamic nitric oxide synthase: comparison with corticotropin-releasing factor and vasopressin gene transcripts. Brain Res. 705, 136-148.
30. Lehner M. and Hartung T. (2002) Endotoxin tolerance-mechanisms and beneficial effects in bacterial infection. Rev. Physiol. Biochem. Pharmacol. 144, 95-141.
31. Luckman S. M., Dyball R. E. and Leng G. (1994) Induction of c-fos expression in hypothalamic magnocellular neurons requires synaptic activation and not simply increased spike activity. J. Neurosci. 14, 4825-4830.
32. Marti O., Garcia A., Vallès A., Harbuz M. S. and Armario A. (2001) Evidence that a single exposure to aversive stimuli triggers longlasting effects in the hypothalamus-pituitary-adrenal axis that consolidate with time. Eur. J. Neurosci. 13, 129-136.
33. Martinez M., Phillips P. J. and Herbert J. (1998) Adaptation in patterns of c-fos expression in the brain associated with exposure to either single or repeated social stress in male rats. Eur. J. Neurosci. 10, 20-33.
34. McKellar S. and Loewy A. D. (1981) Organization of some brain stem afferents to the paraventricular nucleus of the hypothalamus in the rat. Brain Res. 217, 351-357.
35. Melia K. R., Ryabinin A. E., Schroeder R., Bloom F. E. and Wilson M. C. (1994) Induction and habituation of immediate early gene expression in rat brain by acute and repeated restraint stress. J. Neurosci. 14, 5929-5938.
36. Nadeau S. and Rivest S. (1999) Regulation of the gene encoding tumor necrosis factor α (TNF-α) in the rat brain and pituitary in response in different models of systemic immune challenge. J. Neuropathol. Exp. Neurol. 58, 61-77.
37. Nadeau S. and Rivest S. (2000) Role of microglial-derived tumor necrosis factor in mediating CD14 transcription and nuclear factor κB activity in the brain during endotoxemia. J. Neurosci. 20, 3456-3468.
38. Palsson-McDermott E. M. and O'Neill L. A. (2004) Signal transduction by the lipopolysaccharide receptor, Toll-like receptor-4. Immunology 113, 153-162.
39. Paxinos G. and Watson C. (1998) The Rat Brain in Stereotaxic Coordinates, 4th edn. Academic Press, San Diego.
40. Poltorak A., He X., Smirnova I. et al. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282, 2085-2088.
41. Pozzoli G., Costa A., Grimaldi M., Schettini G., Preziosi P., Grossman A. and Navarra P. (1994) Lipopolysaccharide modulation of eicosanoid and corticotrophin-releasing hormone release from rat hypothalamic explants and astrocyte cultures in vitro: evidence for the involvement of prostaglandin E2 but not prostaglandin F2α and lack of effect of nerve growth factor. J. Endocrinol. 140, 103-109.
42. Prewitt C. M. and Herman J. P. (1998) Anatomical interactions between the central amygdaloid nucleus and the hypothalamic paraventricular nucleus of the rat: a dual tract-tracing analysis. J. Chem. Neuroanat. 15, 173-185.
43. Qureshi S. T., Gros P. and Malo D. (1999) Host resistance to infection: genetic control of lipopolysaccharide responsiveness by TOLL-like receptor genes. Trends Genet. 15, 291-294.
44. Rivest S. and Laflamme N. (1995) Neuronal activity and neuropeptide gene transcription in the brains of immune-challenged rats. J. Neuroendocrinol. 7, 501-525.
45. Robertson L. M., Kerppola T. K., Vendrell M., Luk D., Smeyne R. J., Bocchiaro C., Morgan J. I. and Curran T. (1995) Regulation of c-fos expression in transgenic mice requires multiple interdependent transcription control elements. Neuron 14, 241-252.
46. Sawchenko P. E. and Swanson L. W. (1982) The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res. 257, 275-325.
47. Sawchenko P. E., Brown E. R., Chan R. K., Ericsson A., Li H. Y., Roland B. L. and Kovacs K. J. (1996) The paraventricular nucleus of the hypothalamus and the functional neuroanatomy of visceromotor responses to stress. Prog. Brain Res. 107, 201-222.
48. Schmidt E. D., Janszen A. W. J. W., Wouterlood F. G. and Tilders F. J. H. (1995) Interleukin-1-induced long-lasting changes in hypothalamic corticotropin-releasing hormone (CRH)-neurons and hyperresponsiveness of the hypothalamus-pituitary-adrenal axis. J. Neurosci. 15, 7417-7426.
49. Senba E. and Ueyama T. (1997) Stress-induced expression of immediate early genes in the brain and peripheral organs of the rat. Neurosci. Res. 29, 183-207.
50. Simmons D. M., Arriza J. L. and Swanson L. W. (1989) A complete protocol for in situ hybridization of messenger RNAs in brain and other tissues with radio-labeled single-stranded RNA probes. J. Histotechnol. 12, 169-181.
51. Tkacs N. C. and Li J. (1999) Immune stimulation induces Fos expression in brainstem amygdala afferents. Brain Res. Bull. 48, 223-231.
52. Umemoto S., Kawai Y. and Senba E. (1994a) Differential regulation of IEGs in the rat PVH in single and repeated stress models. Neuroreport 6, 201-204.
53. Umemoto S., Noguchi K., Kawai Y. and Senba E. (1994b) Repeated stress reduces the subsequent stress-induced expression of Fos in rat brain. Neurosci. Lett. 167, 101-104.
54. Umemoto S., Kawai Y., Ueyama T. and Senba E. (1997) Chronic glucocorticoid administration as well as repeated stress affects the subsequent acute immobilization stress-induced expression of immediate early genes but not that of NGFI-A. Neuroscience 80, 763-773.
55. Vallès A., Marti O., Harbuz M. S. and Armario A. (2002) A single lipopolysaccharide administration is sufficient to induce a long-term desensitization of the hypothalamic-pituitary-adrenal axis. Neuroscience 112, 383-389.
56. Vallès A., Marti O. and Armario A. (2003) Long-term effects of a single exposure to immobilization stress on the hypothalamic-pituitary-adrenal axis: transcriptional evidence for a progressive desensitization process. Eur. J. Neurosci. 18, 1353-1361.
57. Vallières L. and Rivest S. (1997) Regulation of the genes encoding interleukin-6, its receptor, and gp130 in the rat brain in response to the immune activator lipopolysaccharide and the proinflamatory cytokine interleukin-1β. J. Neurochem. 69, 1668-1683.
58. Vallières L. and Rivest S. (1999) Interleukin-6 is a needed proinflamatory cytokine in the prolonged neural activity and trancriptional activation of corticotropin-releasing factor during endotoxemia. Endocrinology 140, 3890-3903.
59. Viau V. and Sawchenko P. E. (2002) Hypophysiotropic neurons of the paraventricular nucleus respond in spatially, temporally, and phenotypically differentiated manners to acute vs. repeated restraint stress. J. Comp. Neurol. 445, 293-307.
60. Wan W., Janz L., Vriend C. Y., Sorensen C. M., Greenberg A. H. and Nance D. M. (1993) Differential induction of c-Fos immunoreactivity in hypothalamus and brain stem nuclei following central and peripheral administration of endotoxin. Brain Res. Bull. 32, 581-587.
61. Watanabe Y., Stone E. and McEwen B. S. (1994) Induction and habituation of c-fos and zif/268 by acute and repeated stressors. Neuroreport 5, 1321-1324.
62. Watkins L. R., Wiertelak E. P., Goehler L. E., Mooney-Heiberger K., Martine Z. J., Furness L., Smith K. P. and Maier S. F. (1994) Neurocircuitry of illness-induced hyperalgesia. Brain Res. 639, 283-299.
63. Zaldivar N. M. and Scher I. (1979) Endotoxin lethality and tolerance in mice: analysis with the B-lymphocyte-defective CBA/N strain. Infect. Immun. 24, 127-131.