Adaptive changes in acetylcholinesterase gene expression as mediators of recovery from chemical and biological insults

Toxicology

Volumn 233, Issue 1-3 SPEC. ISS., 2007, Pages 97-107

  Evron, Tama ^a   Greenberg, David ^a   Mor, Tsafrir S ^b   Soreq, Hermona ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Acetylcholinesterase; Body temperature; Gene expression; Motor activity; Paraoxon

Indexed keywords

ACETYLCHOLINESTERASE; BACTERIUM LIPOPOLYSACCHARIDE; CHEMICAL WARFARE AGENT; CORTICOSTERONE; LIPOPOLYSACCHARIDE; ORGANOPHOSPHATE; PARAOXON;

ANIMAL CELL; APOPTOSIS; ARTICLE; BACTERIAL INFECTION; CARBOXY TERMINAL SEQUENCE; CENTRAL NERVOUS SYSTEM; CHOLINERGIC SYSTEM; CONTROLLED STUDY; ENZYME BLOOD LEVEL; ENZYME MECHANISM; EXPOSURE; GENE EXPRESSION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HEMATOPOIETIC CELL; MALE; MOTOR ACTIVITY; MOUSE; NEUROMUSCULAR SYSTEM; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; APOPTOSIS; CHO CELLS; CHOLINESTERASE INHIBITORS; CHOLINESTERASES; CORTICOSTERONE; CRICETINAE; CRICETULUS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED STRAINS; MOTOR ACTIVITY; PARAOXON; PEPTIDE FRAGMENTS;

BACTERIA (MICROORGANISMS);

EID: 33947621251     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2006.08.018     Document Type: Article

References (60)

1. Allon N., Rabinovitz I., Manistersky E., Weissman B.A., and Grauer E. Acute and long-lasting cardiac changes following a single whole-body exposure to sarin vapor in rats. Toxicol. Sci. 87 (2005) 385-390
2. Atanasova E., Chiappa S., Wieben E., and Brimijoin S. Novel messenger RNA and alternative promoter for murine acetylcholinesterase. J. Biol. Chem. 274 (1999) 21078-21084
3. Bernik T.R., Friedman S.G., Ochani M., DiRaimo R., Ulloa L., Yang H., Sudan S., Czura C.J., Ivanova S.M., and Tracey K.J. Pharmacological stimulation of the cholinergic antiinflammatory pathway. J. Exp. Med. 195 (2002) 781-788
4. Birikh K.R., Sklan E.H., Shoham S., and Soreq H. Interaction of "readthrough" acetylcholinesterase with RACK1 and PKCbeta II correlates with intensified fear-induced conflict behavior. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 283-288
5. Bon S., Coussen F., and Massoulie J. Quaternary associations of acetylcholinesterase. II. The polyproline attachment domain of the collagen tail. J. Biol. Chem. 272 (1997) 3016-3021
6. Borovikova L.V., Ivanova S., Zhang M., Yang H., Botchkina G.I., Watkins L.R., Wang H., Abumrad N., Eaton J.W., and Tracey K.J. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405 (2000) 458-462
7. Boutsiouki P., and Clough G.F. Modulation of microvascular function following low-dose exposure to the organophosphorous compound malathion in human skin in vivo. J. Appl. Physiol. 97 (2004) 1091-1097
8. Brenner T., Hamra-Amitay Y., Evron T., Boneva N., Seidman S., and Soreq H. The role of readthrough acetylcholinesterase in the pathophysiology of myasthenia gravis. FASEB J. 17 (2003) 214-222
9. Brown L.M., Blair A., Gibson R., Everett G.D., Cantor K.P., Schuman L.M., Burmeister L.F., Van Lier S.F., and Dick F. Pesticide exposures and other agricultural risk factors for leukemia among men in Iowa and Minnesota. Cancer Res. 50 (1990) 6585-6591
10. Browne R.O., Moyal-Segal L.B., Zumsteg D., David Y., Kofman O., Berger A., Soreq H., and Friedman A. Coding region paraoxonase polymorphisms dictate accentuated neuronal reactions in chronic, sub-threshold pesticide exposure. FASEB J. 20 (2006) 1733-1735
11. Cohen O., Erb C., Ginzberg D., Pollak Y., Seidman S., Shoham S., Yirmiya R., and Soreq H. Neuronal overexpression of 'readthrough' acetylcholinesterase is associated with antisense-suppressible behavioral impairments. Mol. Psychiatry 7 (2002) 874-885
12. Cohen O., Reichenberg A., Perry C., Ginzberg D., Pollmacher T., Soreq H., and Yirmiya R. Endotoxin-induced changes in human working and declarative memory associate with cleavage of plasma "readthrough" acetylcholinesterase. J. Mol. Neurosci. 21 (2003) 199-212
13. Deutsch V.R., Pick M., Perry C., Grisaru D., Hemo Y., Golan-Hadari D., Grant A., Eldor A., and Soreq H. The stress-associated acetylcholinesterase variant AChE-R is expressed in human CD34(+) hematopoietic progenitors and its C-terminal peptide ARP promotes their proliferation. Exp. Hematol. 30 (2002) 1153-1161
14. Dori A., Cohen J., Silverman W.F., Pollack Y., and Soreq H. Functional manipulations of acetylcholinesterase splice variants highlight alternative splicing contributions to murine neocortical development. Cereb. Cortex 15 (2005) 419-430
15. Dyer S.M., Cattani M., Pisaniello D.L., Williams F.M., and Edwards J.W. Peripheral cholinesterase inhibition by occupational chlorpyrifos exposure in Australian termiticide applicators. Toxicology 169 (2001) 177-185
16. Evron T., BenMoyal-Segal L., Lam N., Geffen A., and Soreq H. RNA-targeted suppression of stress-induced allostasis in primate spinal cord neurons. Neurodegen. Dis. 2 (2005) 16-27
17. Geyer, B.C., Muralidharan, M., Cherni, I., Doran, J., Fletcher, S.P., Evron, T., Soreq, H., Mor, T.S., 2005. Purification of transgenic plant-derived recombinant human acetylcholinesterase-R. Chem. Biol. Interact.
18. Golier J., and Yehuda R. Neuroendocrine activity and memory-related impairments in posttraumatic stress disorder. Dev. Psychopathol. 10 (1998) 857-869
19. Gordon C.J., and Padnos B.K. Prolonged elevation in blood pressure in the unrestrained rat exposed to chlorpyrifos. Toxicology 146 (2000) 1-13
20. Grisaru D., Deutsch V., Shapira M., Pick M., Sternfeld M., Melamed-Book N., Kaufer D., Galyam N., Gait M.J., Owen D., Lessing J.B., Eldor A., and Soreq H. ARP, a peptide derived from the stress-associated acetylcholinesterase variant, has hematopoietic growth promoting activities. Mol. Med. 7 (2001) 93-105
21. Grisaru D., Pick M., Perry C., Sklan E.H., Almog R., Goldberg I., Naparstek E., Lessing J.B., Soreq H., and Deutsch V. Hydrolytic and nonenzymatic functions of acetylcholinesterase comodulate hemopoietic stress responses. J. Immunol. 176 (2006) 27-35
22. Karczmar A.G. Synaptic, behavioral and toxicological effects of cholinesterase inhibitors in animals and humans. In: Giacobini E. (Ed). Cholineaterases and Cholinesterase Inhibitors (2000), Martin Dunitz, London 157-180
23. Kaufer D., Friedman A., Seidman S., and Soreq H. Acute stress facilitates long-lasting changes in cholinergic gene expression. Nature 393 (1998) 373-377
24. Kaufer D., Friedman A., Seidman S., and Soreq H. Anticholinesterases induce multigenic transcriptional feedback response suppressing cholinergic neurotransmission. Chem. Biol. Interact. 119-120 (1999) 349-360
25. Kawashima K., and Fujii T. The lymphocytic cholinergic system and its biological function. Life Sci. 72 (2003) 2101-2109
26. Kawashima K., and Fujii T. The lymphocytic cholinergic system and its contribution to the regulation of immune activity. Life Sci. 74 (2003) 675-696
27. Lev-Lehman E., Evron T., Broide R.S., Meshorer E., Ariel I., Seidman S., and Soreq H. Synaptogenesis and myopathy under acetylcholinesterase overexpression. J. Mol. Neurosci. 14 (2000) 93-105
28. Li Y., Camp S., Rachinsky T.L., Getman D., and Taylor P. Gene structure of mammalian acetylcholinesterase. Alternative exons dictate tissue-specific expression. J. Biol. Chem. 266 (1991) 23083-23090
29. Luo Z.D., Camp S., Mutero A., and Taylor P. Splicing of 5′ introns dictates alternative splice selection of acetylcholinesterase pre-mRNA and specific expression during myogenesis. J. Biol. Chem. 273 (1998) 28486-28495
30. Maes M., Song C., Lin A., De Jongh R., Van Gastel A., Kenis G., Bosmans E., De Meester I., Benoy I., Neels H., Demedts P., Janca A., Scharpe S., and Smith R.S. The effects of psychological stress on humans: increased production of pro-inflammatory cytokines and a Th1-like response in stress-induced anxiety. Cytokine 10 (1998) 313-318
31. Marrs T.C. Organophosphate poisoning. Pharmacol. Ther. 58 (1993) 51-66
32. Meshorer E., Biton I.E., Ben-Shaul Y., Ben-Ari S., Assaf Y., Soreq H., and Cohen Y. Chronic cholinergic imbalances promote brain diffusion and transport abnormalities. FASEB J. 19 (2005) 910-922
33. Meshorer E., and Soreq H. Virtues and woes of AChE alternative splicing in stress-related neuropathologies. Trends Neurosci. 29 (2006) 216-224
34. Meshorer E., Toiber D., Zurel D., Sahly I., Dori A., Cagnano E., Schreiber L., Grisaru D., Tronche F., and Soreq H. Combinatorial complexity of 5′ alternative acetylcholinesterase transcripts and protein products. J. Biol. Chem. 279 (2004) 29740-29751
35. Metz C.N., and Tracey K.J. It takes nerve to dampen inflammation. Nat. Immunol. 6 (2005) 756-757
36. Nijholt I., Farchi N., Kye M., Sklan E.H., Shoham S., Verbeure B., Owen D., Hochner B., Spiess J., Soreq H., and Blank T. Stress-induced alternative splicing of acetylcholinesterase results in enhanced fear memory and long-term potentiation. Mol. Psychiatry 9 (2004) 174-183
37. Ohno K., Brengman J.M., Felice K.J., Cornblath D.R., and Engel A.G. Congenital end-plate acetylcholinesterase deficiency caused by a nonsense mutation and an A → G splice-donor-site mutation at position + 3 of the collagenlike-tail-subunit gene (COLQ): how does G at position + 3 result in aberrant splicing?. Am. J. Hum. Genet. 65 (1999) 635-644
38. Park S.E., Kim N.D., and Yoo Y.H. Acetylcholinesterase plays a pivotal role in apoptosome formation. Cancer Res. 64 (2004) 2652-2655
39. Perrier A.L., Massoulie J., and Krejci E. PRiMA: the membrane anchor of acetylcholinesterase in the brain. Neuron 33 (2002) 275-285
40. Perry C., Sklan E.H., Birikh K., Shapira M., Trejo L., Eldor A., and Soreq H. Complex regulation of acetylcholinesterase gene expression in human brain tumors. Oncogene 21 (2002) 8428-8441
41. Perry C., Sklan E.H., and Soreq H. CREB regulates AChE-R-induced proliferation of human glioblastoma cells. Neoplasia 6 (2004) 279-286
42. Pick M., Flores-Flores C., and Soreq H. From brain to blood: alternative splicing evidence for the cholinergic basis of Mammalian stress responses. Ann. NY Acad. Sci. 1018 (2004) 85-98
43. Pick M., Perry C., Lapidot T., Guimaraes-Sternberg C., Naparstek E., Deutsch V., and Soreq H. Stress-induced cholinergic signaling promotes inflammation-associated thrombopoiesis. Blood 107 (2006) 3397-3406
44. Pollak Y., Gilboa A., Ben-Menachem O., Ben-Hur T., Soreq H., and Yirmiya R. Acetylcholinesterase inhibitors reduce brain and blood interleukin-1beta production. Ann. Neurol. 57 (2005) 741-745
45. Romanovsky A.A., Almeida M.C., Aronoff D.M., Ivanov A.I., Konsman J.P., Steiner A.A., and Turek V.F. Fever and hypothermia in systemic inflammation: recent discoveries and revisions. Front Biosci. 10 (2005) 2193-2216
46. Rosenstock L., Keifer M., Daniell W.E., McConnell R., and Claypoole K. Chronic central nervous system effects of acute organophosphate pesticide intoxication. The Pesticide Health Effects Study Group. Lancet 338 (1991) 223-227
47. Salmon A., Erb C., Meshorer E., Ginzberg D., Adani Y., Rabinovitz I., Amitai G., and Soreq H. Muscarinic modulations of neuronal anticholinesterase responses. Chem. Biol. Interact. 157-158 (2005) 105-113
48. Seidman S., Sternfeld M., Ben Aziz-Aloya R., Timberg R., Kaufer-Nachum D., and Soreq H. Synaptic and epidermal accumulations of human acetylcholinesterase are encoded by alternative 3′-terminal exons. Mol. Cell Biol. 15 (1995) 2993-3002
49. Shapira M., Tur-Kaspa I., Bosgraaf L., Livni N., Grant A.D., Grisaru D., Korner M., Ebstein R.P., and Soreq H. A transcription-activating polymorphism in the ACHE promoter associated with acute sensitivity to anti-acetylcholinesterases. Hum. Mol. Genet. 9 (2000) 1273-1281
50. Sklan, E.H., Berson, A., Birikh, K., Gutnick, A., Shemesh, O., Shoham, S., Soreq, H., in press. Acetylcholinesterase accentuates stress-induced motor response choices. Biol. Psychiatry.
51. Sklan E.H., Podoly E., and Soreq H. RACK1 has the nerve to act: structure meets function in the nervous system. Prog. Neurobiol. 78 (2006) 117-134
52. Smith E.G., and Gordon C.J. The effects of chlorpyrifos on blood pressure and temperature regulation in spontaneously hypertensive rats. Basic Clin. Pharmacol. Toxicol. 96 (2005) 503-511
53. Soreq H., and Seidman S. Acetylcholinesterase-new roles for an old actor. Nat. Rev. Neurosci. 2 (2001) 294-302
54. Sternfeld M., Ming G., Song H., Sela K., Timberg R., Poo M., and Soreq H. Acetylcholinesterase enhances neurite growth and synapse development through alternative contributions of its hydrolytic capacity, core protein, and variable C termini. J. Neurosci. 18 (1998) 1240-1249
55. Svensson I., Waara L., Johansson L., Bucht A., and Cassel G. Soman-induced interleukin-1 beta mRNA and protein in rat brain. Neurotoxicology 22 (2001) 355-362
56. Taylor P. Agents acting at the neuromuscular junction and autonomic ganglia. In: Hardman J.G., and Limbird L.E. (Eds). In Goodman & Gilman's The Pharmacological Basis of Therapeutics (1996), McGraw-Hill, New York 177-197
57. Tracey K.J., Czura C.J., and Ivanova S. Mind over immunity. FASEB J. 15 (2001) 1575-1576
58. Velan B., Kronman C., Grosfeld H., Leitner M., Gozes Y., Flashner Y., Sery T., Cohen S., Ben-Aziz R., Seidman S., et al. Recombinant human acetylcholinesterase is secreted from transiently transfected 293 cells as a soluble globular enzyme. Cell Mol. Neurobiol. 11 (1991) 143-156
59. Wang H., Yu M., Ochani M., Amella C.A., Tanovic M., Susarla S., Li J.H., Yang H., Ulloa L., Al-Abed Y., Czura C.J., and Tracey K.J. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421 (2003) 384-388
60. Zhang X.J., Yang L., Zhao Q., Caen J.P., He H.Y., Jin Q.H., Guo L.H., Alemany M., Zhang L.Y., and Shi Y.F. Induction of acetylcholinesterase expression during apoptosis in various cell types. Cell Death Differ. 9 (2002) 790-800