The use of null mutant mice to study complex learning and memory processes

Behavior Genetics

Volumn 26, Issue 3, 1996, Pages 301-312

  Wehner, Jeanne M ^a   Bowers, Barbara J ^a   Paylor, Richard ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Ca2+ calmodulin kinase II; Complex learning; hippocampus; null mutants; protein kinase C; transcriptional factors

Indexed keywords

PROTEIN KINASE C; TRANSCRIPTION FACTOR;

GENE TARGETING; GENETIC RECOMBINATION; HIPPOCAMPUS; LEARNING; MEMORY; MOUSE; NONHUMAN; REVIEW;

ANIMALS; BRAIN; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; DNA MUTATIONAL ANALYSIS; GENE TARGETING; HIPPOCAMPUS; LEARNING; LONG-TERM POTENTIATION; MEMORY; MICE; MICE, KNOCKOUT; MICE, NEUROLOGIC MUTANTS; TRANSCRIPTION FACTORS;

ANIMALIA; MAMMALIA;

EID: 0030018512     PISSN: 00018244     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02359386     Document Type: Review

References (88)

1. Abeliovich, A., Chen, C., Goda, Y., Silva, A. J., Stevens, C. F., and Tonegawa, S. (1993a). Modified hippocampal long term potentiation in PKCγ mutant mice. Cell 75: 1253-1262.
2. Abeliovich, A., Paylor, R., Chen, C., Kim, J. J., Wehner, J. M., and Tonegawa, S. (1993b). PKCγ mutant mice exhibit mild deficits in spatial and contextual learning. Cell 75:1263-1271.
3. Akers, R. F., Lovinger, D. M., Colley, P. A., Linder, D. J., and Routtenberg, A. (1986). Translocation of protein kinase C activity may mediate hippocampal long-term potentiation. Science 231:587-589.
4. Anokhin, K. V., and Rose, S. P. R. (1991). Learning-induced increase of immediate early gene messenger RNA in the chick forebrain. Eur. J. Neurosci. 3:162-167.
5. Armstrong, R. C., and Montminy, M. R. (1993). Transsynaptic control of gene expression. In Cowan, W. M., Shooter, E. M., Stevens, C. F., and Thompson, R. F. (eds.), Annual Review of Neuroscience, Annual Reviews Inc., Palo Alto, CA, Vol. 16, pp. 17-30.
6. Bank, B. DeWeer, A., Kuzirian, A. M., Rasmussen, H., and Alkon, D. L. (1988). Classical conditioning induces long-term translocation of protein kinase C in rabbit hippocampal CA1 cells. Proc. Natl. Acad. Sci. USA 85:1988-1992.
7. Bank, B., LoTurco, J. J., and Alkon, D. L. (1989). Learning-induced activation of protein kinase C. A molecular memory trace. Mol. Neurobiol. 3:55-70.
8. Bradley, A. (1993). Site-directed mutagenesis in the mouse. Recent Prog. Hormone Res. 48:237-251.
9. Brandt, S. J., Niedel, J. E., Bell, R. M., and Young, W. S., III (1987). Distinct patterns of expression of different protein kinase C mRNAs in rat tissues. Cell 49:57-63.
10. Büeler, H., Fischer, M., Lang, Y., Bluethmann, H., Lipp, H.-P., DeArmond, S. J., Prusiner, S. B., Aguet, M., and Weissmann, C. (1992). Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356:577-582.
11. 2+/calmodulin-dependent protein kinase in developing rat brain. J. Neurosci. 10:1788-1798.
12. Byrne, G. W., and Ruddle, F. H. (1989). Multiplex gene regulation: A two-tiered approach to transgene regulation in transgenic mice. Proc. Natl. Acatl. Sci. USA 86:5473-5477.
13. Capecchi, M. R. (1989). Altering the genome by homologous recombination. Science 244:1288-1292.
14. Cohen, N. J., and Squire, L. R. (1980). Preserved learning and retention of pattern-analyzing skill in amnesia: Dissociation of knowing how and knowing that. Science 210: 207-209.
15. Cole, A. J., Saffen, D. W., Baraban, J. M., and Worley, P. F. (1989). Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340:474-476.
16. Costantini, F., and Lacy, E. (1981). Introduction of a rabbit β-globin gene into the mouse germ line. Nature 294:92-94.
17. Eichenbaum, H., Fagan, A., and Cohen, N. J. (1986). Normal olfactory discrimination learning set and facilitation of reversal learning after combined and separate lesions of the fornix and amygdala in rats: Implications for preserved learning in amnesia. J. Neurosci. 6:1876-1884.
18. Eichenbaum, H., Mathews, P., and Cohen, N. J. (1989). Further studies of hippocampal representation during odor discrimination learning. Behav. Neurosci. 103:1207-1216.
19. Eichenbaum, H., Otto, T., and Cohen, N. J. (1992). The hippocampus - What does it do? Behav. Neural Bio. 57:2-36.
20. Fordyce, D. E., and Wehner, J. M. (1993). Effects of aging on spatial learning and hippocampal protein kinase C in mice. Neurobiol. Aging 14:309-317.
21. Freeman, J. H., and Stanton, M. E. (1991). Fimbria-fornix transections disrupt the ontogeny of delayed alternation but not position discrimination in the rat. Behav. Neurosci. 105:386-395.
22. Grant, S. G. N., O'Dell, T. J., Karl, K. A., Stein, P. L., Soriano, P., and Kandel, E. R. (1992). Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science 258:1903-1910.
23. Hashimoto, T., Ase, K., Sawamura, S., Kikkawa, U., Saito, N., Tanaka, C., and Nishizuka, Y. (1988). Postnatal development of a brain-specific subspecies of protein kinase C in rat. J. Neurosci. 8:1678-1683.
24. Hasty, P., Ramirez-Solis, R., Krumlauf, R., and Bradley, A. (1991). Introduction of a subtle mutation into the Hox-2.6 locus in embryonic stem cells. Nature 350:243-246.
25. Hawkins, R. D., Kandel, E. R., and Siegelbaum, S. A. (1993). Learning to modulate transmitter release: Themes and variations in synaptic plasticity. In Cowan, W. M., Shooter, E. M., Stevens, C. F., and Thompson, R. F. (eds.), Annual Review of Neuroscience, Annual Reviews Inc., Palo Alto, CA, Vol. 16, pp. 625-665.
26. Hirsh, R. (1974). The hippocampus and contextual retrieval of information from memory: A theory. Behav. Biol. 12: 421-444.
27. Jaenisch, R., and Mintz, B. (1974). Simian virus 40 DNA sequences in DNA of healthy adult mice derived from preimplantation blastocysts injected with viral DNA. Proc. Natl. Acad. Sci. USA 71:1250-1254.
28. Jaenisch, R., Harbers, K., Schnieke, A., Löhler, J., Chumakov, L, Jähner, D., Grotkopp, D., and Hoffmann, E. (1983). Germline integration of Moloney murine leukemia virus at the Mov13 locus leads to recessive lethal mutation and early embryonic death. Cell 32:209-216.
29. Jarrard, L. E. (1983). Selective hippocampal lesions and behavior: Effects of kainic acid lesions on performance of place and cue tasks. Behav. Neurosci. 97:873-889.
30. Jarrard, L. E. (1993). On the role of the hippocampus in learning and memory in the rat. Behav. Neural Biol. 60:9-26.
31. Johnson, R. S., Spiegelman, B. M., and Papaioannou, V. (1992). Pleiotropic effects of a null mutation in the c-fos protooncogene. Cell 71:577-586.
32. Joyner, A. L., Skarnes, W. C., and Rossant, J. (1989). Production of a mutation in mouse En-2 gene by homologous recombination in embryonic stem cells. Nature 338:153-155.
33. Kennedy, M. B., Bennett, M. K., Bulleit, R. F., Erondu, N. E., Jennings, V. R., Miller, S. G., Molloy, S. S., Patton, B. L., and Schenker, L. J. (1990). Structure and regulation of type II calcium/calmodulin-dependent protein kinase in central nervous system neurons. Cold Spring Harbor Symp. Quant. Biol. LV:101-110.
34. Kim, J. J., and Fanselow, M. S. (1992). Modality-specific retrograde amnesia of fear. Science 256:675-677.
35. 2-microglobulin locus in mouse embryonic stem cells by homologous recombination. Proc. Natl. Acad. Sci. USA 86:8932-8935.
36. Kose, A., Ito, A., Saito, N., and Tanaka, C. (1990). Electron microscopic localization of γ- and βII-subspecies of protein kinase C in rat hippocampus. Brain Res. 518:209-217.
37. Lakso, M., Sauer, B., Mosinger, B., Jr., Lee, E. J., Manning, R. W., Yu, S.-H., Mulder, K. L., and Westphal, H. (1992). Targeted oncogene activation by site-specific recombination in transgenic mice. Proc. Natl. Acad. Sci. USA 89: 6232-6236.
38. α gene transgenic mice. Nature 316:38-42.
39. Malenka, R. C., Kauer, J. A., Perkel, D. J., Mauk, M. D., Kelly, P. T., Nicoll, R. A., and Waxham, M. N. (1989). An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation. Nature 340:554-557.
40. Malinow, R., Schulman, H., and Tsien, R. W. (1989). Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245:862.
41. Mansour, S. L., Thomas, K. R., and Capecchi, M. R. (1988). Disruption of the proto-oncogene int-2 in mouse embryo-derived stem cells: A general strategy for targeting mutations to nonselectable genes. Nature 336:348-352.
42. Messer, W. S., Thomas, G. J., and Hoss, W. (1987). Selectivity of pirenzepine in the central nervous system. II. Differential effects of pirenzepine and scopolamine on performance of a representational memory task. Brain Res. 407: 37-45.
43. Mombaerts, P., Iacomini, J., Johnson, R. S., Herrup, K., Tonegawa, S., and Papaioannou, V. E. (1992). RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68:869-877.
44. Morris, R. G. M. (1981). Spatial localisation does not depend on the presence of local cues. Learn. Motiv. 12:239-260.
45. Morris, R. G. M., Garrud, P., Rawlins, J. N. P., and O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
46. Morris, R. G. M., Anderson, E., Lynch, G. S., and Baudry, M. (1986). Selective impairment of learning and blockage of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319:774-776.
47. Nikolaev, E., Kaminska, B., Tischmeyer, W., Matthies, H., and Kaczmarek, L. (1992a). Induction of expression of genes encoding transcription factors in the rat brain elicited by behavioral training. Brain Res. Bull. 28:479-484.
48. Nikolaev, E., Werka, T., and Kaczmarek, L. (1992b). C-fos protooncogene expression in rat brain after long-term training of two-way active avoidance reaction. Behav. Brain Res. 48:91-94.
49. Nishizuka, Y. (1988). The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334:661-665.
50. O'Keefe, J., and Nadel, L. (1978). The Hippocampus as a Cognitive Map, Clarendon, Oxford.
51. Olds, J. L., Anderson, M. L., McPhie, D. L., Staten, L. D., and Alkon, D. L. (1989). Imaging of memory-specific changes in the distribution of protein kinase C in the hippocampus. Science 245:866-869.
52. Olds, J. L., Golski, S., McPhie, D. L., Olton, D., Mishkin, M., and Alkon, D. L. (1990). Discrimination learning alters the distribution of protein kinase C in the hippocampus of rats. J. Neurosci. 10:3707-3713.
53. Olton, D. S., Becker, J. T., and Handelmann, G. E. (1979). Hippocampus, space, and memory. Behav. Brain Sci. 2: 313-365.
54. Orban, P. C., Chui, D., and Marth, J. D. (1992). Tissue- and site-specific DNA recombination in transgenic mice. Proc. Natl. Acad. Sci. USA 89:6861-6865.
55. Palmiter, R. D., Brinster, R. L., Hammer, R. E., Trumbauer, M. E., Rosenfeld, M. G., Birnberg, N. C., and Evans, R. M. (1982a). Dramatic growth of mice that develop from eggs microinjected with metallothionein-growth hormone fusion genes. Nature 300:611-615.
56. Palmiter, R. D., Chen, H. Y., and Brinster, R. L. (1982b). Differential regulation of metallothionein-thymidine kinase fusion genes in transgenic mice and their offspring. Cell 29:701-710.
57. Palmiter, R. D., Norstedt, G., Gelinas, R. E., Hammer, R. E., and Brinster, R. L. (1983). Metallothionein-human GH fusion genes stimulate growth of mice. Science 222:809-814.
58. Paylor, R., Rudy, J. W., and Wehner, J. M. (1991). Acute phorbol ester treatment improves spatial learning performance in rats. Behav. Brain Res. 45:189-193.
59. Paylor, R., Morrison, S. K., Rudy, J. W., Waltrip, L. T., and Wehner, J. M. (1992). Brief exposure to an enriched environment improves performance on the Morris water task and increases hippocampal cytosolic protein kinase C activity in young rats. Behav. Brain Res. 52:49-59.
60. Paylor, R., Baskall, L., and Wehner, J. M. (1993). Behavioral dissociations between C57BL/6 and DBA/2 mice on learning and memory tasks: A hippocampal-dysfunction hypothesis. Psychobiology 21:11-26.
61. Paylor, R., Johnson, R. S., Papaioannou, V., Spiegelman, B. M., and Wehner, J. M. (1994a). Behavioral assessment of c-fos mice. Brain Res. 651:275-282.
62. Paylor, R., Tracy, R., Wehner, J. M., and Rudy, J. W. (1994b). DBA/2 and C57BL/6 mice differ in contextual-fear but not auditory-fear conditioning. Behav. Neurosci. 108: 810-817.
63. Pezzone, M. A., Lee, W.-S., Hoffman, G. E., and Rabin, B. S. (1992). Induction of c-fos immunoreactivity in the rat forebrain by conditioned and unconditioned aversive stimuli. Brain Res. 597:41-50.
64. Phillips, R. G., and LeDoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106:274-285.
65. Ramirez-Solis, R., Zheng, H., Whiting, J., Krumlauf, R., and Bradley, A. (1993). Hoxb-4 (Hox-2.6) mutant mice show homeotic transformation of a cervical vertebra and defects in the closure of the sternal rudiments. Cell 73: 279-294.
66. Rawlins, J. N. P. (1985). Associations across time: The hippocampus as a temporary memory store. Behav. Brain Sci. 8:479-496.
67. Rose, S. P. R. (1991). How chicks make memories: The cellular cascade from c-fos to dendritic remodelling. Trends Neurosci. 14:390-397.
68. Rudy, J. W., and Sutherland, R. J. (1989). The hippocampal formation is necessary for rats to learn and remember configural discriminations. Behav. Brain Res. 34:97-109.
69. Schuman, E. M., and Madison, D. V. (1991). A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 254:1503-1506.
70. Schwartz, J. H., Calignano, A., and Sacktor, T. C. (1990). The role of protein kinase C in learning and memory in Aplysia. In Ritchie, M. M., Magistretti, P. J., and Bolis, E. L. (eds.), Progress in Cell Research, Elsevier, New York, Vol. 1, pp. 279-286.
71. Shearman, M. S., Shinomura, T., Oda, T., and Nishizuka, Y. (1991). Synaptosomal protein kinase C subspecies. A. Dynamic changes in the hippocampus and cerebellar cortex concomitant with synaptogenesis. J. Neurochem. 56:1255-1262.
72. Silva, A. J., Paylor, R., Wehner, J. M., and Tonegawa, S. (1992a). Impaired spatial learning in α-calcium-calmodulin kinase II mutant mice. Science 257:206-211.
73. Silva, A. J., Stevens, C. F., Tonegawa, S., and Wang, Y. (1992b). Deficient hippocampal long-term potentiation in α-calcium-calmodulin kinase II mutant mice. Science 257:201-211.
74. Smith, A. G. (1992). Mouse embryo stem cells: Their identification, propagation and manipulation. Cell Biol. 3: 385-399.
75. Soderling, T. R., Fukunaga, K., Brickey, D. A., Fong, Y. L., Rich, D. P., Smith, K., and Colbran, R. J. (1991). Molecular and cellular studies on brain calcium/calmodulin-dependent protein kinase II. Prog. Brain Res. 89:169-183.
76. Sutherland, R. J., and Rudy, J. W. (1989). Configural association theory: The role of the hippocampal formation in learning, memory, and amnesia. Psychobiology 17:129-144.
77. Sutherland, R. J., Kolb, B., and Whishaw, I. Q. (1982). Spatial mapping: Definitive disruption by hippocampal or medial frontal cortical damage in the rat. Neurosci. Lett. 31:271-276.
78. Thomas, K. R., and Capccchi, M. R. (1986). Introduction of homologous DNA sequences into mammalian cells induces mutations in the cognate gene. Nature 324:34-38.
79. Thomas, K. R., and Capecchi, M. R. (1990). Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature 346:847-850.
80. Tischmeyer, W., Kaczmarek, L., Strauss, M., Jork, R., and Matthies, H. (1990). Accumulation of c-fos mRNA in rat hippocampus during acquisition of a brightness discrimination. Behav. Neural Biol. 54:165-171.
81. Upchurch, M., and Wehner, J. M. (1988). Differences between inbred strains of mice in Morris water maze performance. Behav. Genet. 18:55-68.
82. Wagner, E. F., Stewart, T. A., and Mintz, B. (1981). The human β-globin gene and a functional viral thymidine kinase gene in developing mice. Proc. Natl. Acad. Sci. USA 78:5016-5020.
83. Wahlsten, D. (1972). Genetic experiments with animal learning: A critical review. Behav. Biol. 7:143-182.
84. Wang, Z.-Q., Ovitt, C., Grigoriadis, A. E., Möhle-Steinlein, U., Rüther, U., and Wagner, E. F. (1992). Bone and haematopoietic defects in mice lacking c-fos. Nature 360: 741-745.
85. Wehner, J. M., and Upchurch, M. (1989). The effects of chronic oxotremorine treatment on spatial learning and tolerance development in mice. Pharm. Biochem. Behav. 32:543-551.
86. Wehner, J. M., Sleight, S., and Upchurch, M. (1990). Hippocampal protein kinase C activity is reduced in poor spatial learners. Brain Res. 523:181-187.
87. Wilmut, I., Hooper, M. L., and Simons, J. P. (1991). Genetic manipulation of mammals and its application in reproductive biology. J. Reprod. Fert. 92:245-279.
88. Zimmer, A., and Gruss, P. (1989). Production of chimaeric mice containing embryonic stem (ES) cells carrying a homoeobox Hox 1.1 allele mutated by homologous recombination. Nature 338:150-156.