Extreme reduction of dipeptidyl peptidase IV activity in F344 rat substrains is associated with various behavioral differences

Physiology and Behavior

Volumn 80, Issue 1, 2003, Pages 123-134

  Karl, Tim ^a   Hoffmann, Torsten ^b   Pabst, Reinhard ^a   Von Hörsten, Stephan ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b PROBIODRUG AG   (Germany)

Author keywords

Anxiety; Basic behavioral phenotyping; Dipeptidyl peptidase IV; Ethanol; F344 rats; Feeding behavior; Memory; Motor function; Nociception; Porsolt swim test; Prepulse inhibition; Substrain comparison

Indexed keywords

ALCOHOL; DIPEPTIDYL PEPTIDASE IV; ENTEROSTATIN; GLUCAGON LIKE PEPTIDE 1; NEUROPEPTIDE Y; SUBSTANCE P;

ALCOHOL CONSUMPTION; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BEHAVIOR; BRAIN FUNCTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; FEEDING BEHAVIOR; FEMALE; FLUID INTAKE; HEALTH; LEARNING; MALE; MEMORY; MOTOR PERFORMANCE; NEUROPHYSIOLOGY; NOCICEPTION; NONHUMAN; OPEN FIELD BEHAVIOR; PASSIVE AVOIDANCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; RAT STRAIN; SEDATION; SENSIBILITY; SOCIAL INTERACTION; STRESS; WEIGHT REDUCTION;

EID: 0141956543     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0031-9384(03)00229-4     Document Type: Article

References (86)

1. Archer J. Tests for emotionality in rats and mice: a review. Anim. Behav. 21:1973;205-235.
2. Bannon A.W., Seda J., Carmouche M., Francis J.M., Norman M.H., Karbon B.et al. Behavioral characterization of neuropeptide Y knockout mice. Brain Res. 868:2000;79-87.
3. Borsini F., Meli A. Is the forced swimming test a suitable model for revealing antidepressant activity? Psychopharmacology (Berl.). 94:1988;147-160.
4. Breivik T., Stephan M., Brabant G.E., Straub R.H., Pabst R., von Horsten S. Postnatal lipopolysaccharide-induced illness predisposes to periodontal disease in adulthood. Brain Behav. Immun. 16:2002;421-438.
5. Broqua P., Wettstein J.G., Rocher M.N., Gauthier-Martin B., Riviere P.J., Junien J.L.et al. Antinociceptive effects of neuropeptide Y and related peptides in mice. Brain Res. 724:1996;25-32.
6. Caine S.B., Geyer M.A., Swerdlow N.R. Hippocampal modulation of acoustic startle and prepulse inhibition in the rat. Pharmacol. Biochem. Behav. 43:1992;1201-1208.
7. Carter R.J., Lione L.A., Humby T., Mangiarini L., Mahal A., Bates G.P.et al. Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J. Neurosci. 19:1999;3248-3257.
8. Chaouloff F., Durand M., Mormede P. Anxiety- and activity-related effects of diazepam and chlordiazepoxide in the rat light/dark and dark/light tests. Behav. Brain Res. 85:1997;27-35.
9. Colmers W.F., Wahlestedt C. The biology of neuropepide Y and related peptides. 1993;Humana Press, Totowa.
10. Costall B., Jones B.J., Kelly M.E., Naylor R.J., Tomkins D.M. Exploration of mice in a black and white test box: validation as a model of anxiety. Pharmacol. Biochem. Behav. 32:1989;777-785.
11. Crawley J.N. Behavioral phenotyping of transgenic and knockout mice: experimental design and evaluation of general health, sensory functions, motor abilities, and specific behavioral tests. Brain Res. 835:1999;18-26.
12. Crawley J.N., Paylor R. A proposed test battery and constellations of specific behavioral paradigms to investigate the behavioral phenotypes of transgenic and knockout mice. Horm. Behav. 31:1997;197-211.
13. Crusio W.E., Schwegler H., Lipp H.P. Radial-maze performance and structural variation of the hippocampus in mice: a correlation with mossy fibre distribution. Brain Res. 425:1987;182-185.
14. De Meester I., Durinx C., Bal G., Proost P., Struyf S., Goossens F.et al. Natural substrates of dipeptidyl peptidase IV. Adv. Exp. Med. Biol. 477:2000;67-87.
15. DeFries J.C., Hegmann J.P., Weir M.W. Open-field behavior in mice: evidence for a major gene effect mediated by the visual system. Science. 154:1966;1577-1579.
16. Denenberg V.H. Open-field behavior in the rat: what does it mean? Ann. N.Y. Acad. Sci. 159:1969;852-859.
17. Dewey W.L., Snyder J.W., Harris L.S., Howes J.F. The effect of narcotics and narcotic antagonists on the tail-flick response in spinal mice. J. Pharm. Pharmacol. 21:1969;548-550.
18. Drucker D.J. Glucagon-like peptides. Diabetes. 47:1998;159-169.
19. Erlanson-Albertsson C., York D. Enterostatin - a peptide regulating fat intake. Obes. Res. 5:1997;360-372.
20. File S.E. The use of social interaction as a method for detecting anxiolytic activity of chlordiazepoxide-like drugs. J. Neurosci. Methods. 2:1980;219-238.
21. File S.E. How good is social interaction as a test of anxiety? Simon P., Soubrié P., Wildlocher D. Animal models of psychiatric disorders. Selected models of anxiety, depression and psychosis. 1988;151-166 Karger, Basel, München, Paris, London, New York, New Delhi, Singapore, Tokyo, Sydney.
22. File S.E. Behavioural detection of anxiolytic action. Elliott J.M., Heal D.J., Marsden C.A. Experimental approaches to anxiety and depression. 1992;25-44 John Wiley, Chichester.
23. File S.E., Hyde J.R. Can social interaction be used to measure anxiety? Br. J. Pharmacol. 62:1978;19-24.
24. File S.E., Seth P. A review of 25 years of the social interaction test. Eur. J. Pharmacol. 463:2003;35-53.
25. Gehlert D.R. Multiple receptors for the pancreatic polypeptide (PP-fold) family: physiological implications. Proc. Soc. Exp. Biol. Med. 218:1998;7-22.
26. Hall C.S. Emotional behavior in the rat: defecation and urination as a measure of individual differences in emotionality. J. Comp. Psychol. 18:1934;385-403.
27. Heilig M. Antisense inhibition of neuropeptide Y (NPY)-Y1 receptor expression blocks the anxiolytic-like action of NPY in amygdala and paradoxically increases feeding. Regul. Pept. 59:1995;201-205.
28. Hildebrandt M., Reutter W., Arck P., Rose M., Klapp B.F. A guardian angel: the involvement of dipeptidyl peptidase IV in psychoneuroendocrine function, nutrition and immune defence. Clin. Sci. (Lond.). 99:2000;93-104.
29. Hogg S. A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacol. Biochem. Behav. 54:1996;21-30.
30. Holscher C., Schmidt W.J. Quinolinic acid lesion of the rat entorhinal cortex pars medialis produces selective amnesia in allocentric working memory (WM), but not in egocentric WM. Behav. Brain Res. 63:1994;187-194.
31. Hopsu-Havu V.K., Glenner G.G. A new dipeptide naphthylamidase hydrolyzing glycyl-prolyl-beta-naphthylamide. Histochemie. 7:1966;197-201.
32. Hua X.Y., Boublik J.H., Spicer M.A., Rivier J.E., Brown M.R., Yaksh T.L. The antinociceptive effects of spinally administered neuropeptide Y in the rat: systematic studies on structure-activity relationship. J. Pharmacol. Exp. Ther. 258:1991;243-248.
33. Jones B.J., Roberts D.J. The quantitative measurement of motor incoordination in naive mice using an accelerating rotarod. J. Pharm. Pharmacol. 20:1968;302-304.
34. Kahne T., Lendeckel U., Wrenger S., Neubert K., Ansorge S., Reinhold D. Dipeptidyl peptidase IV: a cell surface peptidase involved in regulating T cell growth. [review] Int. J. Mol. Med. 4:1999;3-15.
35. Kalra S.P., Dube M.G., Pu S., Xu B., Horvath T.L., Kalra P.S. Interacting appetite-regulating pathways in the hypothalamic regulation of body weight. Endocr. Rev. 20:1999;68-100.
36. Karl T., Chwalisz W., Wedekind D., Hedrich H.J., Hoffmann T., Pabst R.et al. Localization, transmission, spontaneous mutations, and variation of function of the Dpp4 (dipeptidyl-peptidase IV; CD26) gene in rats. Regul. Pept. 2003;. [in press].
37. Karl T., Pabst R., von Horsten S. Behavioral phenotyping of mice in pharmacological and toxicological research. Exp. Toxicol. Pathol. 55:2003;69-83.
38. Kask A., Harro J., von Horsten S., Redrobe J.P., Dumont Y., Quirion R. The neurocircuitry and receptor subtypes mediating anxiolytic-like effects of neuropeptide Y. Neurosci. Biobehav. Rev. 26:2002;259-283.
39. Kask A., Nguyen H.P., Pabst R., von Horsten S. Factors influencing behavior of group-housed male rats in the social interaction test: focus on cohort removal. Physiol. Behav. 74:2001;277-282.
40. Kask A., Nguyen H.P., Pabst R., Von Horsten S. Neuropeptide Y Y1 receptor-mediated anxiolysis in the dorsocaudal lateral septum: functional antagonism of corticotropin-releasing hormone-induced anxiety. Neuroscience. 104:2001;799-806.
41. Kelley D.D. Stress-induced analgesia. Ann. N.Y. Acad. Sci. 467:1986.
42. Kieffer T.J., McIntosh C.H., Pederson R.A. Degradation of glucose-dependent insulinotropic polypeptide and truncated glucagon-like peptide 1 in vitro and in vivo by dipeptidyl peptidase IV. Endocrinology. 136:1995;3585-3596.
43. Kushi A., Sasai H., Koizumi H., Takeda N., Yokoyama M., Nakamura M. Obesity and mild hyperinsulinemia found in neuropeptide Y-Y1 receptor-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 95:1998;15659-15664.
44. Lee C., Rodgers R.J. Antinociceptive effects of elevated plus-maze exposure: influence of opiate receptor manipulations. Psychopharmacology (Berl.). 102:1990;507-513.
45. Lister R.G. The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl.). 92:1987;180-185.
46. Luttinger D., Hernandez D.E., Nemeroff C.B., Prange A.J. Jr. Peptides and nociception. Int. Rev. Neurobiol. 25:1984;185-241.
47. Maes M., De Meester I., Scharpe S., Desnyder R., Ranjan R., Meltzer H.Y. Alterations in plasma dipeptidyl peptidase IV enzyme activity in depression and schizophrenia: effects of antidepressants and antipsychotic drugs. Acta Psychiatr. Scand. 93:1996;1-8.
48. Marguet D., Baggio L., Kobayashi T., Bernard A.M., Pierres M., Nielsen P.F.et al. Enhanced insulin secretion and improved glucose tolerance in mice lacking CD26. Proc. Natl. Acad. Sci. U. S. A. 97:2000;6874-6879.
49. Mechiel Korte S., De Boer S.F. A robust animal model of state anxiety: fear-potentiated behaviour in the elevated plus-maze. Eur. J. Pharmacol. 463:2003;163-175.
50. Mentlein R. Dipeptidyl-peptidase IV (CD26) - role in the inactivation of regulatory peptides. Regul. Pept. 85:1999;9-24.
51. Merlo Pich E., Solfrini V., Marrama P., Tiengo M., Agnati L.F., Carani C. Centrally administered neuropeptide Y fails to increase food intake but enhances hypoalgesia in spontaneously hypertensive rats. Neurosci. Lett. 149:1993;209-212.
52. Millan M.J. The induction of pain: an integrative review. Prog. Neurobiol. 57:1999;1-164.
53. Miyakawa T., Yamada M., Duttaroy A., Wess J. Hyperactivity and intact hippocampus-dependent learning in mice lacking the M1 muscarinic acetylcholine receptor. J. Neurosci. 21:2001;5239-5250.
54. Montgomery K.C. The relation between fear induced by novel stimulation and exploratory behavior. J. Comp. Physiol. Psychol. 48:1958;254-260.
55. Nagakura T., Yasuda N., Yamazaki K., Ikuta H., Yoshikawa S., Asano O.et al. Improved glucose tolerance via enhanced glucose-dependent insulin secretion in dipeptidyl peptidase IV-deficient Fischer rats. Biochem. Biophys. Res. Commun. 284:2001;501-506.
56. Naveilhan P., Hassani H., Lucas G., Blakeman K.H., Hao J.X., Xu X.J.et al. Reduced antinociception and plasma extravasation in mice lacking a neuropeptide Y receptor. Nature. 409:2001;513-517.
57. Paylor R., Crawley J.N. Inbred strain differences in prepulse inhibition of the mouse startle response. Psychopharmacology (Berl.). 132:1997;169-180.
58. Pellow S., Chopin P., File S.E., Briley M. Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods. 14:1985;149-167.
59. Picciotto M.R., Wickman K. Using knockout and transgenic mice to study neurophysiology and behavior. Physiol. Rev. 78:1998;1131-1163.
60. Porsolt R.D., LePichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature. 266:1977;730-732.
61. Post C., Paulsson I. Antinociceptive and neurotoxic actions of substance P analogues in the rat's spinal cord after intrathecal administration. Neurosci. Lett. 57:1985;159-164.
62. Pralong F.P., Corder R., Gaillard R.C. The effects of chronic glucocorticoid excess, adrenalectomy and stress on neuropeptide Y in individual rat hypothalamic nuclei. Neuropeptides. 25:1993;223-231.
63. Prut L., Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 463:2003;3-33.
64. Rehbinder C., Alenius S., Bures J., de las Heras M.L., Greko C., Kroon P.S.et al. FELASA recommendations for the health monitoring of experimental units of calves, sheep and goats. Report of the Federation of European Laboratory Animal Science Associations (FELASA) Working Group on Animal Health. Lab. Anim. 34:2000;329-350.
65. Richter C.P., Campbell K.H. Alcohol taste thresholds and concentrations of solution preferred by rats. Science. 91:1940;507-508.
66. Rubinstein M., Mogil J.S., Japon M., Chan E.C., Allen R.G., Low M.J. Absence of opioid stress-induced analgesia in mice lacking beta-endorphin by site-directed mutagenesis. Proc. Natl. Acad. Sci. U. S. A. 93:1996;3995-4000.
67. Sajdyk T.J., Vandergriff M.G., Gehlert D.R. Amygdalar neuropeptide Y Y1 receptors mediate the anxiolytic-like actions of neuropeptide Y in the social interaction test. Eur. J. Pharmacol. 368:1999;143-147.
68. Satinder K.P. Open-field emotional reactivity and alcohol intake in rats. Pharmacol. Biochem. Behav. 17:1982;961-965.
69. Sedelis M., Hofele K., Auburger G.W., Morgan S., Huston J.P., Schwarting R.K. MPTP susceptibility in the mouse: behavioral, neurochemical, and histological analysis of gender and strain differences. Behav. Genet. 30:2000;171-182.
70. Stephan M., Helfritz F., Pabst R., von Horsten S. Postnatally induced differences in adult pain sensitivity depend on genetics, gender and specific experiences: reversal of maternal deprivation effects by additional postnatal tactile stimulation or chronic imipramine treatment. Behav. Brain Res. 133:2002;149-158.
71. Suzuki S., Augerinos G., Black A.H. Stimulus control of spatial behavior on the eight-arm maze in rats. Learn. Motiv. 11:1980;1-18.
72. Swerdlow N.R., Geyer M.A. Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophr. Bull. 24:1998;285-301.
73. Thiele T.E., Koh M.T., Pedrazzini T. Voluntary alcohol consumption is controlled via the neuropeptide Y Y1 receptor. J. Neurosci. 22:2002;RC208.
74. Thiele T.E., Marsh D.J., Ste Marie L., Bernstein I.L., Palmiter R.D. Ethanol consumption and resistance are inversely related to neuropeptide Y levels. Nature. 396:1998;366-369.
75. Thompson N.L., Hixson D.C., Callanan H., Panzica M., Flanagan D., Faris R.A.et al. A Fischer rat substrain deficient in dipeptidyl peptidase IV activity makes normal steady-state RNA levels and an altered protein. Use as a liver-cell transplantation model. Biochem. J. 273:1991;497-502.
76. Thorsell A., Michalkiewicz M., Dumont Y., Quirion R., Caberlotto L., Rimondini R.et al. Behavioral insensitivity to restraint stress, absent fear suppression of behavior and impaired spatial learning in transgenic rats with hippocampal neuropeptide Y overexpression. Proc. Natl. Acad. Sci. U. S. A. 97:2000;12852-12857.
77. Tiruppathi C., Miyamoto Y., Ganapathy V., Leibach F.H. Genetic evidence for role of DPP IV in intestinal hydrolysis and assimilation of prolyl peptides. Am. J. Physiol. 265:1993;G81-G89.
78. Tracey D.J., Romm M.A., Yao N.N. Peripheral hyperalgesia in experimental neuropathy: exacerbation by neuropeptide Y. Brain Res. 669:1995;245-254.
79. Tsuji E., Misumi Y., Fujiwara T., Takami N., Ogata S., Ikehara Y. An active-site mutation (Gly633→Arg) of dipeptidyl peptidase IV causes its retention and rapid degradation in the endoplasmic reticulum. Biochemistry. 31:1992;11921-11927.
80. von Horsten S., Exton M.S., Voge J., Schult M., Nagel E., Schmidt R.E.et al. Cyclosporine A affects open field behavior in DA rats. Pharmacol. Biochem. Behav. 60:1998;71-76.
81. von Horsten S., Schmitt I., Nguyen H.P., Holzmann C., Schmidt T., Walther T.et al. Transgenic rat model of Huntington's disease. Hum. Mol. Genet. 12:2003;617-624.
82. Wahlestedt C., Pich E.M., Koob G.F., Yee F., Heilig M. Modulation of anxiety and neuropeptide Y-Y1 receptors by antisense oligodeoxynucleotides. Science. 259:1993;528-531.
83. Walsh R.N., Cummins R.A. The open-field test: a critical review. Psychol. Bull. 83:1976;482-504.
84. Watanabe Y., Kojima T., Fujimoto Y. Deficiency of membrane-bound dipeptidyl aminopeptidase IV in a certain rat strain. Experientia. 43:1987;400-401.
85. Wettstein J.G., Earley B., Junien J.L. Central nervous system pharmacology of neuropeptide Y. Pharmacol. Ther. 65:1995;397-414.
86. Zalcman S.S. Interleukin-2 potentiates novelty- and GBR 12909-induced exploratory activity. Brain Res. 899:2001;1-9.