Gene knockout of insulin-regulated aminopeptidase: Loss of the specific binding site for angiotensin IV and age-related deficit in spatial memory

Neurobiology of Learning and Memory

Volumn 93, Issue 1, 2010, Pages 19-30

  Albiston, Anthony L ^a   Fernando, Ruani N ^a   Yeatman, Holly R ^a   Burns, Peta ^a   Ng, Leelee ^a   Daswani, Dina ^a   Diwakarla, Shanti ^a   Pham, Vi ^a   Chai, Siew Yeen ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Aminopeptidase; Angiotensin IV; AT4 receptor; Gene knockout; Hippocampus; Memory

Indexed keywords

AMINOPEPTIDASE; ANGIOTENSIN II [3-8]; GLUCOSE TRANSPORTER 4; INSULIN REGULATED AMINOPEPTIDASE; UNCLASSIFIED DRUG;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BRAIN REGION; CONTROLLED STUDY; EMBRYO; GENE DELETION; IMMUNOHISTOCHEMISTRY; KNOCKOUT GENE; KNOCKOUT MOUSE; MAZE TEST; MEMORY DISORDER; MENTAL TASK; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN FUNCTION; SPATIAL MEMORY; TASK PERFORMANCE;

AGING; ANGIOTENSIN II; ANIMALS; BRAIN; CYSTINYL AMINOPEPTIDASE; GLUCOSE TRANSPORTER TYPE 4; MALE; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, KNOCKOUT; NEUROPSYCHOLOGICAL TESTS; PHENOTYPE; RECEPTORS, ANGIOTENSIN; RECOGNITION (PSYCHOLOGY); SPACE PERCEPTION;

EID: 74649085115     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2009.07.011     Document Type: Article

References (46)

1. Albiston A.L., McDowall S.G., Matsacos D., Sim P., Clune E., Mustafa T., et al. Evidence that the angiotensin IV (AT4) receptor is the enzyme insulin regulated aminopeptidase. Journal of Biological Chemistry 276 (2001) 48263-48266
2. Albiston A.L., Morton C.J., Ng H.L., Pham V., Yeatman H.R., Ye S., et al. Identification and characterization of a new cognitive enhancer based on inhibition of insulin-regulated aminopeptidase. FASEB Journal 22 12 (2008) 4209-4217
3. Albiston A.L., Peck G.R., Yeatman H.R., Fernando R., Ye S., and Chai S.Y. Therapeutic targeting of insulin-regulated aminopeptidase: Heads and tails?. Pharmacology & Therapeutics 116 (2007) 417-427
4. Albiston A.L., Pederson E.S., Burns P., Purcell B., Wright J.W., Harding J.W., et al. Reversal of scopolamine-induced memory deficits by LVV-hemorphin 7 in rats in the passive avoidance and Morris water maze paradigms. Behavioural Brain Research 154 (2004) 239-243
5. Bielsky I.F., Hu S.B., Ren X., Terwilliger E.F., and Young L.J. The V1a vasopressin receptor is necessary and sufficient for normal social recognition: A gene replacement study. Neuron 47 (2005) 503-513
6. Braszko J.J., Kupryszewski G., Witczuk B., and Wisniewski K. Angiotensin II-(3-8)-hexapeptide affects motor activity, performance of passive avoidance and a conditioned avoidance response in rats. Neuroscience 27 (1988) 777-783
7. Brinton R.E., Gee K.W., Wamsley J.K., Davis T.P., and Yamamura H.I. Regional distribution of putative vasopressin receptors in rat brain and pituitary by quantitative autoradiography. Proceedings of the National Academy of Sciences of the United States of America 81 (1984) 7248-7252
8. Chai S.Y., Bastias M.A., Clune E.F., Matsacos D.J., Mustafa T., Lee J.H., et al. Distribution of angiotensin IV binding sites (AT(4) receptor) in the human forebrain, midbrain and pons as visualised by in vitro receptor autoradiography. Journal of Chemical Neuroanatomy 20 (2000) 339-348
9. Chai S.Y., Lee J.H., Matscos D., McDowall S.G., Mendelsohn F.A.O.M., Robel P., et al. Angiotensin AT4 receptor distribution in mouse brain and its possible role in facilitation of spatial memory. Journal of Neurochemistry 78 (2001) 15
10. Chen J.K., Zimpelmann J., Harris R.C., and Burns K.D. Angiotensin IV induces tyrosine phosphorylation of focal adhesion kinase and paxillin in proximal tubule cells. American Journal of Physiology-Renal Physiology 280 (2001) F980-F988
11. Crawley J.N., and Paylor R. A proposed test battery and constellations of specific behavioral paradigms to investigate the behavioral phenotypes of transgenic and knockout mice. Hormones and Behavior 31 (1997) 197-211
12. Davis C.J., Kramár E.A., De A., Meighan P.C., Simasko S.M., Wright J.W., et al. AT4 receptor activation increases intracellular calcium influx and induces a non-N-methyl-d-aspartate dependent form of long-term potentiation. Neuroscience 137 (2006) 1369-1379
13. De Bundel D., Smolders I., Vanderheyden P., and Michotte Y. Ang II and Ang IV: unraveling the mechanism of action on synaptic plasticity, memory, and epilepsy. CNS Neuroscience & Therapeutics 14 (2008) 315-339
14. Fernando R.S.L., Albiston A.L., and Chai S.Y. Sub-cellular localization of insulin-regulated membrane aminopeptidase, IRAP, to vesicles in neurons. Journal of Neurochemistry 102 (2007) 967-976
15. Fernando R.N., Albiston A.L., and Chai S.Y. The insulin-regulated aminopeptidase IRAP is colocalised with GLUT4 in the mouse hippocampus - potential role in modulation of glucose uptake in neurones?. European Journal of Neuroscience 28 (2008) 588-598
16. Fernando R., Larm J., Albiston A.L., and Chai S.Y. Distribution and cellular localization of the insulin regulated aminopeptidase (IRAP) in the rat central nervous system. Journal of Comparative Neurology 487 (2005) 372-390
17. Hanesworth J.M., Sardinia M.F., Krebs L.T., Hall K.L., and Harding J.W. Elucidation of a specific binding site for angiotensin II(3-8), angiotensin IV, in mammalian heart membranes. Journal of Pharmacology and Experimental Therapeutics 266 (1993) 1036-1042
18. Helmig S., Schuckenböhmer P., Heger J., Euler G., Piper H.M., and Schlüter K.D. Direct effects of the angiotensin-converting enzyme inhibitor ramiprilat on adult rat ventricular cardiomyocytes. Acta Physiologica (Oxford) 191 (2007) 267-274
19. Herbst J.J., Ross S.A., Scott H.M., Bobin S.A., Morris N.J., Lienhard G.E., et al. Insulin stimulates cell surface aminopeptidase activity toward vasopressin in adipocytes. American Journal of Physiology 272 (1997) E600-E606
20. Katz E.B., Stenbit A.E., JHatton K., DePinho R., and Charron M.J. Cardiac and adipose tissue abnormalities but not diabetes in mice deficient in GLUT4. Nature 377 (1995) 151-155
21. Keller S.R., Davis A.C., and Clairmont K.B. Mice deficient in the insulin-regulated membrane aminopeptidase show substantial decreases in glucose transporter GLUT4 levels but maintain normal glucose homeostasis. Journal of Biological Chemistry 277 (2002) 17677-17686
22. Keller S.R., Scott H.M., Mastick C.C., Aebersold R., and Lienhard G.E. Cloning and characterization of a novel insulin-regulated membrane aminopeptidase from Glut4 vesicles. Journal of Biological Chemistry 270 (1995) 23612-23618
23. Kohlstedt K., Brandes R.P., Muller-Esterl W., Busse R., and Fleming I. Angiotensin-converting enzyme is involved in outside-in signaling in endothelial cells. Circulation Research 94 (2004) 60-67
24. Landgraf R. The involvement of the vasopressin system in stress-related disorders. CNS Neurological Disorders Drug-Targets 5 (2006) 167-179
25. Larance M., Ramm G., Stockli J., van Dam E.M., Winata S., Wasinger V., et al. Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking. Journal of Biological Chemistry 280 (2005) 37803-37813
26. Lee J., Albiston A.L., Allen A.M., Mendelsohn F.A.O., Ping S.E., Barrett G.L., et al. Effect of intracerebroventricular injection of AT4 receptor ligands, Nle1-angiotensin IV and LVv-hemorphin 7, on spatial learning in rats. Neuroscience 124 (2004) 341-349
27. Lee J.H., Mustafa T., McDowall S.G., Mendelsohn F.A.O., Brennan M.B., Lew R., et al. Structure-activity study of LVV-hemorphin-7: Angiotensin AT4 receptor ligand and inhibitor of insulin-regulated aminopeptidase (IRAP). Journal of Pharmacology and Experimental Therapeutics 305 (2003) 205-211
28. Lew R.A., Mustafa T., Ye S., McDowall S.G., Chai S.Y., and Albiston A.L. Angiotensin AT4 ligands are potent, competitive inhibitors of insulin regulated aminopeptidase (IRAP). Journal of Neurochemistry 86 (2003) 344-350
29. Li Y.D., Block E.R., and Patel J.M. Activation of multiple signaling modules is critical in angiotensin IV-induced lung endothelial cell proliferation. American Journal of Physiology 263 (2002) L707-L716
30. Matsumoto H., Hattori A., Mizutani S., and Tsujimoto M. Cleavage of peptide hormones by placental leucine aminopeptidase/oxytocinase. Cell-surface aminopeptidases: Basic and clinical aspects (2001), Elsevier Science BV
31. McEwen B.B. De Wied and colleagues IV: Research into mechanisms of action by which vasopressin and oxytocin influence memory processing. Advances in Pharmacology 50 (2004) 177-225
32. Mishima K., Tsukikawa H., Miura I., Inada K., Abe K., Matsumoto Y., et al. Ameliorative effect of NC-1900, a new AVP4-9 analog, through vasopressin V1A receptor on scopolamine-induced impairments of spatial memory in the eight-arm radial maze. Neuropharmacology 44 (2003) 541-552
33. Moeller I., Lew R.A., Mendelsohn F.A., Smith A.I., Brennan M.E., Tetaz T.J., et al. The globin fragment LVV-hemorphin-7 is an endogenous ligand for the AT4 receptor in the brain. Journal of Neurochemistry 68 (1997) 2530-2537
34. Ostrowski N.L., Lolait S.J., and Young W.S.R. Cellular localization of vasopressin V1a receptor messenger ribonucleic acid in adult male rat brain, pineal, and brain vasculature. Endocrinology 135 (1994) 1511-1528
35. Peck G.R., Ye S., Pham V., Fernando R.N., Macaulay S.L., Chai S.Y., et al. Interaction of the Akt substrate, AS160, with the glucose transporter 4 vesicle marker protein, insulin-regulated aminopeptidase. Molecular Endocrinology 20 (2006) 2576-2583
36. Pederson E.S., Harding J.W., and Wright J.W. Attenuation of scopolamine-induced spatial learning impairments by an angiotensin IV analog. Regulatory Peptides 74 (1998) 97-103
37. Rogers D.C., Fisher E.M., Brown S.D., Peters J., Hunter A.J., and Martin J.E. Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mammalian Genome 8 (1997) 711-713
38. Schwenk F., Baron U., and Rajewsky K. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Research 23 (1995) 5080-5081
39. Serradeil-Le G.C., Wagnon J., Simiand J., Griebel G., Lacour C., Guillon G., et al. Characterization of (2S,4R)-1-[5-chloro-1-[(2,4-dimethoxyphenyl)sulfonyl]-3-(2-methoxy-phenyl)-2-oxo-2,3-dihydro-1H-indol-3-yl]-4-hydroxy-N,N-dimethyl-2-pyrrolidine carboxamide (SSR149415), a selective and orally active vasopressin V1b receptor antagonist. Journal of Pharmacology and Experimental Therapeutics 300 (2002) 1122-1130
40. Stragier B., De Bundel D., Sarre S., Smolders I., Vauquelin G., Dupont A., et al. Involvement of insulin-regulated aminopeptidase in the effects of the renin-angiotensin fragment angiotensin IV: A review. Heart Failure Review 13 (2008) 321-337
41. Stragier B., Demaegdt H., De Bundel D., Smolders I., Sarre S., Vauquelin G., et al. Involvement of insulin-regulated aminopeptidase and/or aminopeptidase N in the angiotensin IV-induced effect on dopamine release in the striatum of the rat. Brain Research 1131 (2007) 97-105
42. Wallis M.G., Lankford M.F., and Keller S.R. Vasopressin is a physiological substrate for the insulin-regulated aminopeptidase IRAP. American Journal of Physiology-Endocrinology and Metabolism 293 (2007) E1092-E1102
43. Wright J.W., Miller-Wing A.V., Shaffer M.J., Higginson C., Wright D.E., Hanesworth J.M., et al. Angiotensin II(3-8) (ANG IV) hippocampal binding: potential role in the facilitation of memory. Brain Research Bulletin 32 (1993) 497-502
44. Wright J.W., Stubley L., Pederson E.S., Kramar E.A., Hanesworth J.M., and Harding J.W. Contributions of the brain angiotensin IV-AT4 receptor subtype system to spatial learning. Journal of Neuroscience 19 (1999) 3952-3961
45. Wright J.W., Yamamoto B.J., and Harding J.W. Angiotensin receptor subtype mediated physiologies and behaviors: New discoveries and clinical targets. Progress in Neurobiology 84 (2008) 157-181
46. Yang R., Smolders I., De Bundel D., Fouyn R., Halberg M., Demaegdt H., et al. Brain and peripheral angiotensin II type 1 receptors mediate renal vasoconstrictor and blood pressure responses to angiotensin IV in the rat. Journal of Hypertension 26 (2008) 998-1007