Behavioral and genetic investigations of low exploratory behavior in Il18r1-/- mice: We can't always blame it on the targeted gene

Brain, Behavior, and Immunity

Volumn 24, Issue 7, 2010, Pages 1116-1125

  Eisener Dorman, Amy F ^a,b   Lawrence, David A ^a,b   Bolivar, Valerie J ^a,b  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Anxiety; Flanking region; Il18; Il18r; Knockout mouse; Locomotor activity

Indexed keywords

INTERLEUKIN 18; INTERLEUKIN 18 RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME 1; CHROMOSOME 10; CHROMOSOME 14; CHROMOSOME 4; CHROMOSOME 5; CHROMOSOME 8; EXPLORATORY BEHAVIOR; GENE TARGETING; GENETICS; LOCOMOTION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANXIETY; CHROMOSOME MAPPING; DISEASE MODELS, ANIMAL; DNA; EXPLORATORY BEHAVIOR; GENOTYPE; INTERLEUKIN-18; INTERLEUKIN-18 RECEPTOR ALPHA SUBUNIT; MICE; MICE, CONGENIC; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, KNOCKOUT; MOTOR ACTIVITY; PHENOTYPE; POLYMERASE CHAIN REACTION; SPECIES SPECIFICITY;

EID: 80053302109     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2010.05.002     Document Type: Article

References (72)

1. Airey D.C., Lu L., Williams R.W. Genetic control of the mouse cerebellum: identification of quantitative trait loci modulating size and architecture. J. Neurosci. 2001, 21:5099-5109.
2. Arend W.P., Palmer G., Gabay C. IL-1, IL-18, and IL-33 families of cytokines. Immunol. Rev. 2008, 223:20-38.
3. Bolivar V.J. Intrasession and intersession habituation in mice: from inbred strain variability to linkage analysis. Neurobiol. Learn. Mem. 2009, 92:206-214.
4. Bolivar V., Flaherty L. A region on chromosome 15 controls intersession habituation in mice. J. Neurosci. 2003, 23:9435-9438.
5. Bolivar V.J., Caldarone B.J., Reilly A.A., Flaherty L. Habituation of activity in an open field: a survey of inbred strains and F1 hybrids. Behav. Genet. 2000, 30:285-293.
6. Bolivar V.J., Cook M.N., Flaherty L. Mapping of quantitative trait loci with knockout/congenic strains. Genome Res. 2001, 11:1549-1552.
7. Bolivar V.J., Ganus J.S., Messer A. The development of behavioral abnormalities in the motor neuron degeneration (mnd) mouse. Brain Res. 2002, 937:74-82.
8. Bolivar V.J., Manley K., Messer A. Exploratory activity and fear conditioning abnormalities develop early in R6/2 Huntington's disease transgenic mice. Behav. Neurosci. 2003, 117:1233-1242.
9. Bolivar V.J., Manley K., Messer A. Early exploratory behavior abnormalities in R6/1 Huntington's disease transgenic mice. Brain Res. 2004, 1005:29-35.
10. Bossu P., Ciaramella A., Salani F., Bizzoni F., Varsi E., Di Iulio F., Giubilei F., Gianni W., Trequattrini A., Moro M.L., Bernardini S., Caltagirone C., Spalletta G. Interleukin-18 produced by peripheral blood cells is increased in Alzheimer's disease and correlates with cognitive impairment. Brain Behav. Immun. 2008, 22:487-492.
11. Bothe G.W., Bolivar V.J., Vedder M.J., Geistfeld J.G. Genetic and behavioral differences among five inbred mouse strains commonly used in the production of transgenic and knockout mice. Genes Brain Behav. 2004, 3:149-157.
12. Bothe G.W., Bolivar V.J., Vedder M.J., Geistfeld J.G. Behavioral differences among fourteen inbred mouse strains commonly used as disease models. Comp. Med. 2005, 55:326-334.
13. Bouwknecht J.A., Paylor R. Pitfalls in the interpretation of genetic and pharmacological effects on anxiety-like behaviour in rodents. Behav. Pharmacol. 2008, 19:385-402.
14. Cannella B., Raine C.S. Multiple sclerosis: cytokine receptors on oligodendrocytes predict innate regulation. Ann. Neurol. 2004, 55:46-57.
15. Conti B., Park L.C.H., Calingasan N.Y., Kim Y., Kim H., Bae Y., Gibson G.E., Joh T.H. Cultures of astrocytes and microglia express interleukin 18. Mol. Brain Res. 1999, 67:46-52.
16. Cook M.N., Williams R.W., Flaherty L. Anxiety-related behaviors in the elevated zero-maze are affected by genetic factors and retinal degeneration. Behav. Neurosci. 2001, 115:468-476.
17. Cook M.N., Bolivar V.J., McFadyen M.P., Flaherty L. Behavioral differences among 129 substrains: implications for knockout and transgenic mice. Behav. Neurosci. 2002, 116:600-611.
18. Crawley J. What's Wrong With My Mouse? Behavioral Phenotyping of Transgenic and Knockout Mice 2007, Wiley-Interscience, Hoboken, NJ.
19. Crusio W.E. Flanking gene and genetic background problems in genetically manipulated mice. Biol. Psychiatry 2004, 56:381-385.
20. Cryan J.F., Holmes A. The ascent of mouse: advances in modelling human depression and anxiety. Nat. Rev. Drug Discov. 2005, 4:775-790.
21. Culhane A.C., Hall M.D., Rothwell N.J., Luheshi G.N. Cloning of rat brain interleukin-18 cDNA. Mol. Psychiatry 1998, 3:362-366.
22. Cumiskey D., Curran B.P., Herron C.E., O'Connor J.J. A role for inflammatory mediators in the IL-18 mediated attenuation of LTP in the rat dentate gyrus. Neuropharmacology 2007, 52:1616-1623.
23. Curran B., O'Connor J.J. The pro-inflammatory cytokine interleukin-18 impairs long-term potentiation and NMDA receptor-mediated transmission in the rat hippocampus in vitro. Neuroscience 2001, 108:83-90.
24. Danciger M., Lyon J., Worrill D., LaVail M.M., Yang H. A strong and highly significant QTL on chromosome 6 that protects the mouse from age-related retinal degeneration. Invest. Ophthalmol. Vis. Sci. 2003, 44:2442-2449.
25. Dinarello C.A., Novick D., Puren A.J., Fantuzzi G., Shapiro L., Muhl H., Yoon D.Y., Reznikov L.L., Kim S.H., Rubinstein M. Overview of interleukin-18: more than an interferon-gamma inducing factor. J. Leukoc. Biol. 1998, 63:658-664.
26. Eisener-Dorman A.F., Lawrence D.A., Bolivar V.J. Cautionary insights on knockout mouse studies: the gene or not the gene?. Brain Behav. Immun. 2009, 23:318-324.
27. Felderhoff-Mueser U., Schmidt O.I., Oberholzer A., Buhrer C., Stahel P.F. IL-18: a key player in neuroinflammation and neurodegeneration?. Trends Neurosci. 2005, 28:487-493.
28. File, S.E., Lippa, A.S., Beer, B., Lippa, M.T., 2004. Animal tests of anxiety. Curr Protoc Neurosci (Chapter 8, Unit 8.3).
29. Flaherty L. Congenic strains. The Mouse in Biomedical Research 1981, 215-222. Academic Press, New York. H.L. Foster, J.D. Small, J.G. Fox (Eds.).
30. Flaherty L., Bolivar V. Congenic and consomic strains. Neurobehavioral Genetics: Methods and Applications 2007, 115-127. CRC Press, Boca Raton. B.C. Jones, P. Mormede (Eds.).
31. Gerlai R. Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype?. Trends Neurosci. 1996, 19:177-181.
32. Gill K.J., Boyle A.E. Confirmation of quantitative trait loci for cocaine-induced activation in the AcB/BcA series of recombinant congenic strains. Pharmacogenetics 2003, 13:329-338.
33. Gill K.J., Boyle A.E. Quantitative trait loci for novelty/stress-induced locomotor activation in recombinant inbred (RI) and recombinant congenic (RC) strains of mice. Behav. Brain Res. 2005, 161:113-124.
34. Gutcher I., Urich E., Wolter K., Prinz M., Becher B. Interleukin 18-independent engagement of interleukin 18 receptor-alpha is required for autoimmune inflammation. Nat. Immunol. 2006, 7:946-953.
35. Hedtjarn M., Leverin A.L., Eriksson K., Blomgren K., Mallard C., Hagberg H. Interleukin-18 involvement in hypoxic-ischemic brain injury. J. Neurosci. 2002, 22:5910-5919.
36. Hoshino K., Tsutsui H., Kawai T., Takeda K., Nakanishi K., Takeda Y., Akira S. Cutting edge: generation of IL-18 receptor-deficient mice: evidence for IL-1 receptor-related protein as an essential IL-18 binding receptor. J. Immunol. 1999, 162:5041-5044.
37. Kalueff A.V., Wheaton M., Murphy D.L. What's wrong with my mouse model? Advances and strategies in animal modeling of anxiety and depression. Behav. Brain Res. 2007, 179:1-18.
38. Kirstein S.L., Davidson K.L., Ehringer M.A., Sikela J.M., Erwin V.G., Tabakoff B. Quantitative trait loci affecting initial sensitivity and acute functional tolerance to ethanol-induced ataxia and brain cAMP signaling in BXD recombinant inbred mice. J. Pharmacol. Experiment. Therapeut. 2002, 302:1238-1245.
39. Kubota T., Fang J., Brown R.A., Krueger J.M. Interleukin-18 promotes sleep in rabbits and rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 281:R828-R838.
40. Lamkanfi M., Dixit V.M. Inflammasomes: guardians of cytosolic sanctity. Immunol. Rev. 2009, 227:95-105.
41. Martinon F., Mayor A., Tschopp J. The inflammasomes: guardians of the body. Annu. Rev. Immunol. 2009, 27:229-265.
42. McFadyen M.P., Kusek G., Bolivar V.J., Flaherty L. Differences among eight inbred strains of mice in motor ability and motor learning on a rotorod. Genes Brain Behav. 2003, 2:214-219.
43. Meziane H., Ouagazzal A.M., Aubert L., Wietrzych M., Krezel W. Estrous cycle effects on behavior of C57BL/6J and BALB/cByJ female mice: implications for phenotyping strategies. Genes Brain Behav. 2007, 6:192-200.
44. Mill J., Galsworthy M.J., Paya-Cano J.L., Sluyter F., Schalkwyk L.C., Plomin R., Asherson P. Home-cage activity in heterogeneous stock (HS) mice as a model of baseline activity. Genes Brain Behav. 2002, 1:166-173.
45. Mori I., Hossain M.J., Takeda K., Okamura H., Imai Y., Kohsaka S., Kimura Y. Impaired microglial activation in the brain of IL-18-gene-disrupted mice after neurovirulent influenza A virus infection. Virology 2001, 287:163-170.
46. Nadel L. Dorsal and ventral hippocampal lesions and behavior. Physiol. Behav. 1968, 3:891-900.
47. Nakamura K., Okamura H., Wada M., Nagata K., Tamura T. Endotoxin-induced serum factor that stimulates gamma interferon production. Infect. Immun. 1989, 57:590-595.
48. Nakamura K., Xiu Y., Ohtsuji M., Sugita G., Abe M., Ohtsuji N., Hamano Y., Jiang Y., Takahashi N., Shirai T., Nishimura H., Hirose S. Genetic dissection of anxiety in autoimmune disease. Hum. Molecul. Genet. 2003, 12:1079-1086.
49. Nishihara E., Tsaih S.W., Tsukahara C., Langley S., Sheehan S., DiPetrillo K., Kunita S., Yagami K., Churchill G.A., Paigen B., Sugiyama F. Quantitative trait loci associated with blood pressure of metabolic syndrome in the progeny of NZO/HILtJxC3H/HeJ intercrosses. Mamm. Genome 2007, 18:573-583.
50. Ojala J., Alafuzoff I., Herukka S.K., van Groen T., Tanila H., Pirttila T. Expression of interleukin-18 is increased in the brains of Alzheimer's disease patients. Neurobiol. Aging 2009, 30:198-209.
51. Okamura H., Tsutsi H., Komatsu T., Yutsudo M., Hakura A., Tanimoto T., Torigoe K., Okura T., Nukada Y., Hattori K., et al. Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature 1995, 378:88-91.
52. Qiao H., Sonoda K.H., Sassa Y., Hisatomi T., Yoshikawa H., Ikeda Y., Murata T., Akira S., Ishibashi T. Abnormal retinal vascular development in IL-18 knockout mice. Lab. Invest. 2004, 84:973-980.
53. Qiao H., Sonoda K.H., Ikeda Y., Yoshimura T., Hijioka K., Jo Y.J., Sassa Y., Tsutsumi-Miyahara C., Hata Y., Akira S., Ishibashi T. Interleukin-18 regulates pathological intraocular neovascularization. J. Leukoc. Biol. 2007, 81:1012-1021.
54. Rodriques de Ledesma A.M., Desai A.N., Bolivar V.J., Symula D.J., Flaherty L. Two new behavioral QTLs, Emo4 and Reb1, map to mouse Chromosome 1: congenic strains and candidate gene identification studies. Mamm. Genome 2006, 17:111-118.
55. Sharma S., Kulk N., Nold M.F., Graf R., Kim S.H., Reinhardt D., Dinarello C.A., Bufler P. The IL-1 family member 7b translocates to the nucleus and down-regulates proinflammatory cytokines. J. Immunol. 2008, 180:5477-5482.
56. Shimomura K., Low-Zeddies S.S., King D.P., Steeves T.D., Whiteley A., Kushla J., Zemenides P.D., Lin A., Vitaterna M.H., Churchill G.A., Takahashi J.S. Genome-wide epistatic interaction analysis reveals complex genetic determinants of circadian behavior in mice. Genome Res. 2001, 11:959-980.
57. Simpson E.M., Linder C.C., Sargent E.E., Davisson M.T., Mobraaten L.E., Sharp J.J. Genetic variation among 129 substrains and its importance for targeted mutagenesis in mice. Nat. Genet. 1997, 16:19-27.
58. Singer J.B., Hill A.E., Nadeau J.H., Lander E.S. Mapping quantitative trait loci for anxiety in chromosome substitution strains of mice. Genetics 2005, 169:855-862.
59. Sugama S., Cho B.P., Baker H., Joh T.H., Lucero J., Conti B. Neurons of the superior nucleus of the medial habenula and ependymal cells express IL-18 in rat CNS. Brain Res. 2002, 958:1-9.
60. Sugama S., Wirz S.A., Barr A.M., Conti B., Bartfai T., Shibasaki T. Interleukin-18 null mice show diminished microglial activation and reduced dopaminergic neuron loss following acute 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine treatment. Neuroscience 2004, 128:451-458.
61. Sugama S., Fujita M., Hashimoto M., Conti B. Stress induced morphological microglial activation in the rodent brain: involvement of interleukin-18. Neuroscience 2007, 146:1388-1399.
62. Sugiyama F., Churchill G.A., Higgins D.C., Johns C., Makaritsis K.P., Gavras H., Paigen B. Concordance of murine quantitative trait loci for salt-induced hypertension with rat and human loci. Genomics 2001, 71:70-77.
63. Takeda K., Tsutsui H., Yoshimoto T., Adachi O., Yoshida N., Kishimoto T., Okamura H., Nakanishi K., Akira S. Defective NK cell activity and Th1 response in IL-18-deficient mice. Immunity 1998, 8:383-390.
64. Tang X., Sanford L.D. Home cage activity and activity-based measures of anxiety in 129P3/J, 129X1/SvJ and C57BL/6J mice. Physiol. Behav. 2005, 84:105-115.
65. Wang S.S., Shi W., Wang X., Velky L., Greenlee S., Wang M.T., Drake T.A., Lusis A.J. Mapping, genetic isolation, and characterization of genetic loci that determine resistance to atherosclerosis in C3H mice. Arterioscler. Thromb. Vasc. Biol. 2007, 27:2671-2676.
66. Williams R.W., Airey D.C., Kulkarni A., Zhou G., Lu L. Genetic dissection of the olfactory bulbs of mice: QTLs on four chromosomes modulate bulb size. Behav. Genet. 2001, 31:61-77.
67. Wolf N., Galecki A., Lipman R., Chen S., Smith-Wheelock M., Burke D., Miller R. Quantitative trait locus mapping for age-related cataract severity and synechia prevalence using four-way cross mice. Invest. Ophthalmol. Vis. Sci. 2004, 45:1922-1929.
68. Wolfer D.P., Crusio W.E., Lipp H.P. Knockout mice: simple solutions to the problems of genetic background and flanking genes. Trends Neurosci. 2002, 25:336-340.
69. Yaguchi T., Nagata T., Yang D., Nishizaki T. Interleukin-18 regulates motor activity, anxiety and spatial learning without affecting synaptic plasticity. Behav. Brain Res. 2010, 206:47-51.
70. Zhang S., Lou Y., Amstein T.M., Anyango M., Mohibullah N., Osoti A., Stancliffe D., King R., Iraqi F., Gershenfeld H.K. Fine mapping of a major locus on chromosome 10 for exploratory and fear-like behavior in mice. Mamm. Genome 2005, 16:306-318.
71. Zorrilla E.P., Sanchez-Alavez M., Sugama S., Brennan M., Fernandez R., Bartfai T., Conti B. Interleukin-18 controls energy homeostasis by suppressing appetite and feed efficiency. Proc. Natl. Acad. Sci. USA 2007, 104:11097-11102.
72. Zwijnenburg P.J., van der Poll T., Florquin S., Akira S., Takeda K., Roord J.J., van Furth A.M. Interleukin-18 gene-deficient mice show enhanced defense and reduced inflammation during pneumococcal meningitis. J. Neuroimmunol. 2003, 138:31-37.