Peptides and aging: Their role in anorexia and memory

Peptides

Volumn 72, Issue , 2015, Pages 112-118

  Morley, John E ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anorexia of aging; Cognitive decline; Frailty; Memory; Neuropeptides; Peptides

Indexed keywords

ALPHA INTERMEDIN; AMYLOID BETA PROTEIN; CHOLECYSTOKININ; DYNORPHIN; GHRELIN; GLUCAGON LIKE PEPTIDE 1; NEUROPEPTIDE; PEPTIDE; PEPTIDE HORMONE;

AGING; ALZHEIMER DISEASE; ANOREXIA; ARTICLE; CONCENTRATION (PARAMETERS); HUMAN; MEMORY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; ANIMAL; COGNITION; METABOLISM;

AGING; ANIMALS; ANOREXIA; COGNITION; HUMANS; MEMORY; PEPTIDE HORMONES;

EID: 84947047698     PISSN: 01969781     EISSN: 18735169     Source Type: Journal    
DOI: 10.1016/j.peptides.2015.04.007     Document Type: Article

References (148)

1. Ortman JM, Velkoft VA, Hogan H. An aging nation: The older population in the United States. www.census.gov/prod/2014pubs/p25-1140pdf [accessed 2/16/15].
2. J.E. Morley, B. Vellas, G.A. van Kan, S.D. Anker, J.M. Bauer, R. Bernabei, and et al. Frailty consensus: A call to action J Am Med Dir Assoc 14 2013 392 397
3. J.P. Michel Sarcopenia: there is a need for some steps forward J Am Med Dir Assoc 15 2014 379 380
4. J.E. Morley Developing novel therapeutic approaches to frailty Curr Pharm Des 15 2009 3384 3395
5. J.E. Morley Pathophysiology of the anorexia of aging Curr Opin Clin Nutr Metab Care 16 2013 27 32
6. J.E. Morley Anorexia of aging: a true geriatric syndrome J Nutr Health Aging 16 2012 422 425
7. J.E. Morley, J.F. Flood, H.M. Perry III, and V.B. Kumar Peptides, memory, food intake and aging Aging (Milano) 9 4 Suppl 1997 17 18
8. J.E. Morley, V.B. Kumar, A.E. Bernardo, S.A. Farr, K. Uezu, N. Tumosa, and et al. Beta-amyloid precursor polypeptide in SAMP8 mice affects learning and memory Peptides 21 2000 1761 1767
9. V.B. Kumar, S.A. Farr, J.F. Flood, V. Kamlesh, M. Franko, W.A. Banks, and et al. Site-directed antisense oligonucleotide decreases the expression of amyloid precursor protein and reverses deficits in learning and memory in aged SAMP8 mice Peptides 21 2000 1769 1775
10. J.E. Morley New horizons in the management of Alzheimer disease J Am Med Dir Assoc 16 2015 1 5
11. F. Mir, F. Zafar, and J.E. Morley Anorexia of aging: can we decrease protein energy undernutrition in the nursing home? J Am Med Dir Assoc 14 2013 77 79
12. J.E. Morley Weight loss in older persons: new therapeutic approaches Curr Pharm Des 13 2007 3637 3647
13. J.E. Morley, and A.J. Silver Anorexia in the elderly Neurobiol Aging 9 1988 9 16
14. W.K. Clarkson, M.M. Pantano, J.E. Morley, M. Horowitz, J.M. Littlefield, and F.R. Burton Evidence for the anorexia of aging: gastrointestinal transit and hunger in healthy elderly vs. young adults Am J Physiol 272 1 Pt 2 1997 R243 R248
15. I.M. Chapman, C.G. MacIntosh, J.E. Morley, and M. Horowitz The anorexia of ageing Biogerontology 3 2002 67 71
16. K.L. Jones, S.M. Doran, K. Hveem, F.D. Bartholomeusz, J.E. Morley, W.M. Sun, and et al. Relation between postprandial satiation and antral area in normal subjects Am J Clin Nutr 66 1997 127 132
17. K. Sturm, B. Parker, J. Wishart, C. Feinle-Bisset, K.L. Jones, I. Chapman, and et al. Energy intake and appetite are related to antral area in healthy young and older subjects Am J Clin Nutr 80 2004 656 667
18. A.J. Silver, J.F. Flood, A.M. Song, and J.E. Morley Evidence for a physiological role for CCK in the regulation of food intake in mice Am J Physiol 256 3 Pt 2 1989 R646 R652
19. A.J. Silver, and J.E. Morley Role of CCK in regulation of food intake Prog Neurobiol 36 1991 23 34
20. J.E. Morley, A.S. Levine, J. Kneip, and M. Grace The effect of vagotomy on the satiety effects of neuropeptides and naloxone Life Sci 30 1982 1943 1947
21. A.I. Sayegh The role of cholecystokin receptors in the short-term control of food intake Prog Mol Biol Transl Sci 144 2013 277 316
22. A.J. Silver, J.F. Flood, and J.E. Morley Effect of gastrointestinal peptides on ingestion in old and young mice Peptides 9 1988 221 225
23. M. Balaskó, S. Soós, A. Párniczky, M. Koncsecskó-Gáspár, M. Székely, and E. Pétarvári Anorexic effect of peripheral cholecystokinin (CCK) varies with age and body composition (short communication) Acta Physiol Hung 99 2012 166 172
24. C.G. McIntosh, M. Horowitz, M.A. Verhagen, A.J. Smout, J. Wishart, H. Morris, and et al. Effect of small intestinal nutrient infusion on appetite, gastrointestinal hormone release, and gastric myoelectrical activity in young and older men Am J Gastroenterol 96 2001 997 1007
25. M. Serra Prat, E. Mans, E. Paolmera, and P. Clavé Gastrointestinal Motil 25 2013 e245 e291
26. C.G. MacIntosh, J.E. Morley, J. Wishart, H. Morris, J.B. Jansen, M. Horowitz, and et al. Effect of exogenous cholecystokinin (CCK)-8 on food intake and plasma CCK, leptin, and insulin concentrations in older and young adults: Evidence for increased CCK activity as a cause of the anorexia of aging J Clin Endocrinol Metab 86 2001 5830 5837
27. F.S. Gaskin, S.A. Farr, W.A. Banks, V.B. Kumar, and J.E. Morley Ghrelin-induced feeding is dependent on nitric oxide Peptides 24 2003 913 918
28. K. Toshinai, M.S. Mondal, T. Shimbara, H. Yamaguchi, Y. Date, K. Hangawa, and et al. Ghrelin stimulates growth hormone secretion and food intake in aged rats Mech Ageing Dev 128 2007 182 186
29. S. Gilg, and T.A. Lutz The orexigenic effect of peripheral ghrelin differs between rats of different age and with different baseline food intake, and it may in part be mediated by the area postrema Physiol Behav 87 2006 353 359
30. S. Akimoto, and K. Miyasaka Age-associated changes of appetite-regulating peptides Geriatr Gerontol Int 10 Suppl 1 2010 S107 S119
31. R. Nass, L.S. Farhy, J. Liu, S.S. Pezzoli, M.L. Johnson, B.D. Gaylinn, and et al. Age-dependent decline in acyl-ghrelin concentrations and reduced association of acyl-ghrelin and growth hormone in healthy older adults J Clin Endocrinol Metab 99 2014 602 608
32. J. Kozakowski, M. Rabijewski, and W. Zgliczyński Ghrelin-growth hormone releasing and orexigenic hormone in men declines with age, insulin and with decrease in testosterone concentration Neuro Endocrinol Lett 29 2008 100 106
33. J.M. Bauer, A. Haack, K. Winning, R. Wirth, B. Rischer, W. Uter, and et al. Impaired postprandial response of active ghrelin and prolonged suppression of hunger sensation in the elderly J Gerontol A Biol Sci Med Sci 65 2010 307 311
34. S.M. Schneider, R. Al-Jaouni, C. Caruba, J. Giudicelli, K. Arab, F. Suavet, and et al. Effects of age, malnutrition and refeeding on the expression and secretion of ghrelin Clin Nutr 27 2008 724 731
35. J.M. Garcia, R.V. Boccia, C.D. Graham, Y. Yan, E.M. Duus, S. Allen, and et al. Anamorelin for patients with cancer cachexia: an integrated analysis of two phase 2 randomised, placebo-controlled, double-blind trials Lancet Oncol 16 2015 108 116
36. J.E. Morley, S. von Haehling, and S.D. Anker Are we closer to having drugs to treat muscle wasting disease? J Cachexia Sarcopenia Muscle 5 2014 83 87
37. A. Lastya, M.R. Saraswati, and K. Suastika The low level of glucagon-like peptide-1 (glp-1) is a risk factor of type 2 diabetes mellitus BMC Res Notes 7 849 2014
38. J.E. Morley, P.M. Morley, and J.F. Flood Anorectic effects of amylin in rats over the life span Pharmacol Biochem Behav 44 1993 577 580
39. J.E. Morley, H.M. Perry III, R.P. Baumgartner, and P.J. Garry Leptin, adipose tissue and aging - is there a role for testosterone? J Gerontol A Biol Sci Med Sci 54 1999 B108 B109
40. R.N. Baumgartner, R.R. Ross, D.L. Waters, W.M. Brooks, J.E. Morley, G.D. Montoya, and et al. Serum leptin in elderly people: associations with sex hormones, insulin, and adipose tissue volumes Obes Res 7 1999 141 149
41. J.E. Morley Decreased food intake with aging J Gerontol A Biol Sci Med Sci 56 Spec 2 2001 81 88
42. J.E. Morley, and A.S. Levine Involvement of dynorphin and the kappa opioid receptor in feeding Peptides 4 1983 797 800
43. B.A. Gosnell, A.S. Levine, and J.E. Morley The effects of aging on opioid modulation of feeding in rats Life Sci 32 1983 2793 2799
44. C.G. MacIntosh, J. Sheehan, N. Davani, J.E. Morley, M. Horowitz, and I.M. Chapman Effects of aging on the opioid modulation of feeding in humans J Am Geriatr Soc 49 2001 1518 1524
45. M. Martinez, A. Hernanz, J. Gómez-Cerezo, J.M. Peña, J.J. Vazquez, and F. Arnalich Alterations in plasma and cerebrospinal fluid levels of neuropeptides in idiopathic senile anorexia Regul Pept 49 1993 109 117
46. T. Wolden-Hanson, B.T. Marck, and A.M. Matsumoto Blunted hypothalmic neuropeptide gene expression in response to fasting, but preservation of feeding responses to AgRP in aging male Brown Norway rats Am J Physiol Regul Integr Comp Physiol 287 2004 R138 R146
47. E.H. Sohn, T. Wolden-Hanson, and A.M. Matsumoto Testosterone (T)-induced changes in arcuate nucleus cocaine-amphetamine-regulated transcript and NPY mRNA are attenuated in old compared to young male brown Norway rats: Contribution of T to age-related changes in cocaine-amphetamine-regulated transcript and NPY gene expression Endocrinology 143 2002 954 963
48. E. Pétervári, A.O. Szabad, S. Soós, A. Garami, M. Székely, and M. Balaskó Central alpha-MSH infusion in rats: disparate anorexic vs. metabolic changes with aging Regul Pept 166 2011 105 111
49. E. Pétervári, A. Garami, S. Soós, M. Székely, and M. Balaskó Age-dependence of alpha-MSH-induced anorexia Neuropeptides 44 2010 315 322
50. Y.H. Choi, C. Li, K. Page, A. Westby, M.A. Della-Fera, J. Lin, and et al. Melanocortin receptors mediate leptin effects on feeding and body weight but not adipose apoptosis Physiol Behav 79 4-5 2003 795 801
51. J.E. Morley, E.N. Hernandez, and J.F. Flood Neuropeptide Y increases food intake in mice Am J Physiol 253 3 Pt 2 1987 R516 R522
52. J.E. Morley Orexigenic and anabolic agents Clin Geriatr Med 18 2002 853 866
53. M.K. Hellerstein, S.N. Meydani, M. Meydani, K. Wu, and C.A. Dinarello Interleukin-1-induced anorexia in the rat. Influence of prostaglandins J Clin Invest 84 1989 223 235
54. M. Michaud, L. Balardy, G. Moulis, C. Gaudin, C. Peyrot, B. Vellas, and et al. Proinflammatory cytokines, aging, and age-related diseases J Am Med Dir Assoc 14 2013 877 882
55. S. Soenen, and I.M. Chapman Body weight, anorexia, and undernutrition in older people J Am Med Dir Assoc 14 2013 642 648
56. M. Thakur, and D.G. Blazer Depression in long-term care J Am Med Dir Assoc 9 2008 82 87
57. J.E. Morley Depression in nursing home residents J Am Med Dir Assoc 11 2010 301 303
58. J.E. Morley, and A.S. Levine Corticotrophin releasing factor, grooming and ingestive behavior Life Sci 31 1982 1459 1464
59. R.B. Lloyd, and C.B. Nemeroff The role of corticotropin-releasing hormone in the pathophysiology of depression: therapeutic implications Curr Top Med Chem 11 2011 609 617
60. C.M. Banki, G. Bissette, M. Arato, L. O'Connor, and C.B. Nemeroff CSF corticotropin-releasing factor-like immunoreactivity in depression and schizophrenia Am J Psychiatr 144 1987 873 877
61. J.E. Morley Cognition and nutrition Curr Opin Nutr Metab Care 17 2014 1 4
62. J.E. Morley Mild cognitive impairment - a treatable condition J Am Med Dir Assoc 15 2014 1 5
63. J.E. Morley Dementia: does vitamin D modulate cognition? Nat Rev Neurol 10 2014 613 614
64. J.F. Flood, G.E. Smith, and J.E. Morley Modulation of memory processing by cholecystokinin: dependence on the vagus nerve Science 236 1987 832 834
65. J.F. Flood, M.O. Merbaum, and J.E. Morley The memory enhancing effects of cholecystokinin octapeptide are dependent on an intact stria terminalis Neurobiol Learn Mem 64 1995 139 145
66. C. Hadjiivanova, S. Belcheva, and I. Belcheva Cholecystokinin and learning and memory processes Acta Physiol Pharmacol Bulg 27 2003 83 88
67. J.F. Flood, J.S. Garland, and J.E. Morley Evidence that cholecystokinin-enhanced retention is mediated by changes in opioid activity in the amygdala Brain Res 585 1992 94 104
68. J.F. Flood, and J.E. Morley Effects of bombesin and gastrin-releasing peptide on memory processing Brain Res 460 1988 314 322
69. J.F. Flood, and J.E. Morley Cholecystokinin receptors mediate enhanced memory retention produced by feeding and gastrointestinal peptides Peptides 10 1989 809 813
70. E.C. McNay Insulin and ghrelin: peripheral hormones modulating memory and hippocampal function Curr Opin Pharmacol 7 2007 628 632
71. J.E. Morley, J.F. Flood, S.A. Farr, H.J. Perry III, F.E. Kaiser, and P.M. Morley Effects of amylin on appetite regulation and memory Can J Physiol Pharmacol 73 1995 1042 1046
72. J.F. Flood, J.E. Morley, and K. Tatemoto Effects of systemic pancreastatin on memory retention Peptides 9 1988 1077 1080
73. J.F. Flood, and J.E. Morley Differential effects of amylin on memory processing using peripheral and central routes of administration Peptides 13 1992 577 580
74. S. Diano, S.A. Farr, S.C. Benoit, E.C. McNay, I. da Silva, B. Horvath, and et al. Ghrelin controls hippocampal spine synapse density and memory performance Nat Neurosci 9 2006 381 388
75. V.P. Carlini, M.E. Monzón, M.M. Varas, A.B. Cragnolini, H.B. Schiöth, T.N. Scimonelli, and et al. Ghrelin increases anxiety-like behavior and memory retention in rats Biochem Biophys Res Commun 299 2002 739 743
76. Q. Zhu, K. Xiao, M. Yu, M. Niu, C. Li, Y. Gao, and et al. Ghrelin but not nesfatin-1 affects certain forms of learning and memory in both rats and mice Brain Res 1541 2013 42 51
77. B. Beck, and G. Pourié Ghrelin, neuropeptide Y, and other feeding-regulatory peptides active in the hippocampus: role in learning and memory Nutr Rev 71 2013 541 561
78. V.P. Carlini, M.F. Perez, E. Salde, H.B. Schiöth, O.A. Ramirez, and S.R. de Barioglio Ghrelin induced memory facilitation implicates nitric oxide synthase activation and decrease in the threshold to promote LTP in hippocampal dentate gyrus Physiol Behav 101 2010 117 123
79. B.A. Kent, A.L. Beynon, A.K. Hornsby, P. Bekinschtein, T.J. Bussey, J.S. Davies, and et al. The orexigenic hormone acyl-ghrelin increases adult hippocampal neurogenesis and enhances pattern separation Psychoneuroendocrinology 51 2015 431 439
80. L. Song, Q. Zhu, T. Liu, M. Yu, K. Xiao, Q. Kong, and et al. Ghrelin modulates lateral amygdala neuronal firing and blocks acquisition for conditioned taste aversion PLoS ONE 8 6 2013 e65422
81. M. Alvarez-Crespo, K.P. Skibicka, I. Farkas, C.S. Molnár, E. Egecioglu, E. Hrabovszky, and et al. The amygdala as a neurobiological target for ghrelin in rats: neuroanatomical, electrophysiological and behavioral evidence PLoS ONE 7 10 2012 e46321
82. M.S. Ghersi, L.A. Gabach, F. Buteler, A.A. Vilcaes, H.B. Schiöth, M.F. Perez, and et al. Ghrelin increases memory consolidation through hippocampal mechanisms dependent on glutamate release and NR2B-subunits of the NMDS receptor Psychopharmacology (Berl) 2014 [Epub ahead of print, December 4]
83. M.B.G. Spitznagel, A. Benitez, J. Updegraff, V. Potter, T. Alexander, E. Glickman, and et al. Serum ghrelin is inversely associated with cognitive function in a sample of non-demented elderly Psychiatr Clin Neurosci 64 2010 608 611
84. M.J. During, L. Cao, D.S. Zuzga, J.S. Francis, H.L. Fitzsimons, X. Jiao, and et al. Glucagon-like peptide-1 receptor is involved in learning and neuroprotection Nat Med 9 2003 1173 1179
85. V.A. Gault, W.D. Porter, P.R. Flatt, and C. Hölscher Actions of exendin-4 therapy on cognitive function and hippocampal synaptic plasticity in mice fed a high-fat diet Int J Obes (Lond) 34 2010 1341 1344
86. D. Porter, E. Faivre, P.R. Flatt, C. Hölscher, and V.A. Gault Actions of incretin metabolites on locomotor activity, cognitive function and in vivo hippocampal synaptic plasticity in high fat fed mice Peptides 35 2012 1 8
87. P.L. McClean, and C. Hölscher Liraglutide can reverse memory impairment, synaptic loss and reduce plaque load in aged APP/PS1 mice, a model of Alzheimer's disease Neuropharmacology 76 Pt A 2014 57 67
88. D. Tweedie, L. Rachmany, V. Rubovitch, E. Lehrmann, Y. Zhang, K.G. Becker, and et al. Exendin-4, a glucagon-like peptide-1 receptor agonist prevents mTBI-induced changes in hippocampus gene expression and memory deficits in mice Exp Neurol 239 2013 170 182
89. S.V. Korol, Z. Jin, O. Babateen, and B. Birnir GLP-1 and exendin-4 transiently enhance GABAA receptor-mediated synaptic and tonic currents in rat hippocampal CA3 pyramidal neurons Diabetes 64 2015 79 89
90. V.A. Gault, R. Lennox, and P.R. Flatt Sitagliptin, a dipeptidyl peptidase-4 inhibitor, improves recognition memory, oxidative stress and hippocampal neurogenesis and upregulates key genes involved in cognitive decline Diabetes Obes Metab 7 2015 10.1111/dom.12432 [Epub ahead of print, January 7]
91. S.A. Farr, J.L. Ripley, R. Sultana, Z. Zhang, M.L. Niehoff, T.L. Platt, and et al. Antisense oligonucleotide against GSK-3β in brain of SAMP8 mice improves learning and memory and decreases oxidative stress: Involvement of transcription factor Nrf2 and implications for Alzheimer disease Free Radic Biol Med 67 2014 387 395
92. H.H. Hansen, K. Fabricus, P. Barkholt, M.L. Niehoff, J.E. Morley, J. Jelsing, and et al. The GLP-1 receptor agonist liraglutide improves memory function and increases hippocampal CA1 neuronal numbers in a senescence-accelerated mouse model of Alzheimer's disease J Alzheimer Dis 2015
93. K.E. Sandoval, S.A. Farr, W.A. Banks, M.L. Niehoff, J.E. Morley, A.M. Crider, and et al. Chronic peripheral administration of somatostatin receptor subtype-4 agonist NNC 26-9100 enhances learning and memory in SAMP8 mice Eur J Pharmacol 654 2011 53 59
94. 1-4 2 trimers Eur J Pharmacol 683 2012 116 124
95. S.A. Farr, W.A. Banks, and J.E. Morley Effects of leptin on memory processing Peptides 27 2006 1420 1425
96. Y. Oomura, N. Hori, T. Shiraishi, K. Fukunaga, H. Takeda, M. Tsuji, and et al. Leptin facilitates learning and memory performance and enhances hippocampal CA1 long-term potentiation and CaMK II phosphorylation in rats Peptides 27 2006 2738 2749
97. I. Martins, S. Gomes, R.O. Costa, L. Otvos, C.R. Oliveira, R. Resende, and et al. Leptin and ghrelin prevent hippocampal dysfunction induced by Aβ oligomers Neuroscience 241 2013 41 51
98. A. Perianes-Cachero, E. Burgos-Ramos, L. Puebla-Jiménez, S. Canelles, L.M. Frago, A. Hervás-Aguilar, and et al. Acute up-regulation of the rat brain somatostatin receptor-effector system by leptin is related to activation of insulin signaling and may counteract central leptin actions Neuroscience 252 2013 289 301
99. S.A. Farr, K.A. Yamada, D.A. Butterfield, H.M. Abdul, L. Xu, N.E. Miller, and et al. Obesity and hypertriglyceridemia produce cognitive impairment Endocrinology 149 2008 2628 2636
100. W.A. Banks The blood-brain barrier: connecting the gut and the brain Regul Pept 149 1-3 2008 11 14
101. J.F. Flood, E.N. Hernandez, and J.E. Morley Modulation of memory processing by neuropeptide Y Brain Res 421 1987 280 290
102. J.F. Flood, M.L. Baker, E.N. Hernandez, and J.E. Morley Modulation of memory processing by neuropeptide Y varies with brain injection site Brain Res 503 1989 73 82
103. J.E. Morley, and J.F. Flood Neuropeptide Y and memory processing Ann NY Acad Sci 503 1990 73 82
104. J.F. Flood, M.L. Baker, E.N. Hernandez, and J.E. Morley Modulation of memory retention by neuropeptide K Brain Res 520 1990 284 290
105. L.B. Jaeger, S.A. Farr, W.A. Banks, and J.E. Morley Effects of orexin-A on memory processing Peptides 23 2002 1683 1688
106. S.M. De la Monte Intranasal insulin therapy for cognitive impairment and neurodegeneration: current state of the art Expert Opin Drug Deliv 10 2013 1699 1709
107. J.E. Morley, J.F. Flood, H.M. JIII Perry, and V.B. Kumar Peptides, memory, food intake and aging Aging (Milano) 9 4 Suppl 1997 17 18
108. S.M. de la Monte Intranasal insulin therapy for cognitive impairment and neurodegeneration: current state of the art Expert Opin Drug Deliv 10 2013 1699 1709
109. A. Claxton, L.D. Baker, A. Hanson, E.H. Trittschuh, B. Cholerton, A. Morgan, and et al. Long-acting intranasal insulin detemir improves cognition for adults with mild cognitive impairment or early-stage Alzheimer's disease dementia J Alzheimers Dis 44 2015 897 906
110. S. Maimaiti, K.L. Anderson, C. DeMoll, L.D. Brewer, B.A. Rauh, J.C. Gant, and et al. Intranasal insulin improves age-related cognitive deficits and reverses electrophysiological correlates of brain aging J Gerontol A Biol Sci Med Sci 2015 pii:glu314 [Epub ahead of print, February 6]
111. A.J. Kastin, and W. Pan Blood-brain barrier and feeding: regulatory roles of saturable transport systems for ingestive peptides Curr Pharm Des 14 2008 1615 1619
112. A.J. Kastin, and W. Pan Feeding peptides interact in several ways with the blood-brain barrier Curr Pharm Des 9 2003 789 794
113. A.J. Kastin, W. Pan, L.M. Maness, and W.A. Banks Peptides crossing the blood-brain barrier: some unusual observations Brain Res 848 1999 96 100
114. W.A. Banks, A.J. Kastin, L.M. Maness, M.F. Banks, M. Shayo, and R.N. McLay Interactions of beta-amyloids with the blood-brain barrier Ann NY Acad Sci 826 1997 190 199
115. W.A. Banks, and A.J. Kastin Passage of peptides across the blood-brain barrier: pathophysiological perspectives Life Sci 59 1996 1923 1943
116. J.E. Morley, and S.A. Farr Hormesis and amyloid-β protein: physiology or pathology? J Alzheimer Dis 29 2012 487 492
117. J.E. Morley, S.A. Farr, W.A. Banks, S.N. Johnson, K.A. Yamada, and L. Xu A physiological role for amyloid-beta protein: enhancement of learning and memory J Alzheimer Dis 19 2010 441 449
118. J.E. Morley, and S.A. Farr The role of amyloid-beta in the regulation of memory Biochem Pharmacol 88 2014 479 485
119. D. Puzzo, and O. Arancio Amyloid-β peptide: Dr Jekyll or Mr. Hyde? J Alzheimer Dis 33 Suppl 1 2013 S111 S120
120. J.F. Flood, J.E. Morley, and E. Roberts Amnestic effects in mice of four synthetic peptides homologous to amyloid beta protein from patients with Alzheimer disease Proc Natl Acad Sci USA 88 1991 3363 3366
121. J.F. Flood, E. Roberts, M.A. Sherman, B.E. Kaplan, and J.E. Morley Topography of a binding site for small amnestic peptides deduced from structure-activity studies: relation to amnestic effect of amyloid beta protein Proc Natl Acad Sci USA 91 1994 380 384
122. J.F. Flood, J.E. Morley, and E. Roberts An amyloid beta-protein fragment, a beta[12-28], equipotently impairs post-training memory processing when injected into different limbic system structures Brain Res 14 1994 271 276
123. T. Maurice, B.P. Lockhart, and A. Privat Amnesia induced in mice by centrally administered beta-amyloid peptides involves cholinergic dysfunction Brain Res 706 1996 181 193
124. M. Hiramatsu, K. Inoue, and T. Kameyama Dynorphin A-(1-13) and (2-13) improve beta-amyloid peptide-induced amnesia in mice Neuroreport 11 2000 431 435
125. M.E. Gibbs, D. Maksel, Z. Gibbs, X. Hou, R.J. Summers, and D.H. Small Memory loss caused by beta-amyloid protein is rescued by a beta(3)-adrenoceptor agonist Neurobiol Aging 31 2010 614 624
126. J.E. Morley, S.A. Farr, V.B. Kumar, and H.J. Armbrecht The SAMP8 mouse: a model to develop therapeutic interventions for Alzheimer's disease Curr Pharm Des 18 2012 1123 1130
127. J.F. Flood, and J.E. Morley Age-related changes in footshock avoidance acquisition and retention in senescence accelerated mouse (SAM) Neurobiol Aging 14 1993 153 157
128. T. Takeda, M. Hosokawa, and K. Higuchi Senescence-accelerated mouse (SAM): a novel murine model of senescence Exp Gerontol 32 1-2 1997 105 109
129. M.A. Erickson, M.L. Niehoff, S.A. Farr, J.E. Morley, L.A. Dillman, K.M. Lynch, and et al. Peripheral administration of antisense oligonucleotides targeting the amyloid-β protein precursor reverses AβPP and LRP-1 overexpression in the aged SAMP8 mouse brain J Alzheimer Dis 28 2012 951 960
130. J.E. Morley, S.A. Farr, V.B. Kumar, and W.A. Banks Alzheimer's disease through the eye of a mouse. Acceptance lecture for the 2001 Gayle A. Olson and Richard D. Olson prize Peptides 23 2002 589 599
131. J.E. Morley, H.J. Armbrecht, S.A. Farr, and V.B. Kumar The senescence accelerated mouse (SAMP8) as a model for oxidative stress and Alzheimer's disease Biochim Biophys Acta 1822 5 2012 650 656
132. H.F. Poon, S.A. Farr, V. Thongboonkerd, B.C. Lynn, W.A. Banks, J.E. Morley, and et al. Proteomic analysis of specific brain proteins in aged SAMP8 mice treated with alpha-lipoic acid: implications for aging and age-related neurodegenerative disorders Neurochem Int 46 2005 159 168
133. W.A. Banks, S.M. Robinson, S. Verma, and J.E. Morley Efflux of human and mouse amyloid beta proteins 1-40 and 1-42 from brain: impairment in a mouse model of Alzheimer's disease Neuroscience 121 2003 487 492
134. R. Strong, V. Reddy, and J.E. Morley Cholinergic deficits in the septal-hippocampal pathway of the SAM-P/8 senescence accelerated mouse Brain Res 966 2003 150 156
135. V.B. Kumar, K. Vyas, M. Buddhiraju, M. Alshaher, J.F. Flood, and J.E. Morley Changes in membrane fatty acids and delta-9 desaturase in senescence accelerated (SAMP8) mouse hippocampus with aging Life Sci 65 1999 1657 1662
136. A.L. Petursdottir, S.A. Farr, J.E. Morley, W.A. Banks, and G.V. Skuladottir Lipid peroxidation in brain during aging in the senescence-accelerated mouse (SAM) Neurogiol Aging 28 2007 1170 1178
137. J.F. Flood, J.E. Morley, and M. La Reginna Age-related changes in the pharmacological improvement of retention in senescence accelerated mouse (SAM) Neurobiol Aging 14 1993 159 166
138. J.F. Flood, S.A. Farr, F.E. Kaiser, M. La Regina, and J.E. Morley Age-related decrease of plasma testosterone in SAMP8 mice: replacement improves age-related impairment of learning and memory Physiol Behav 57 1995 669 673
139. J.E. Morley, S.A. Farr, and J.F. Flood Antibody to amyloid beta protein alleviates impaired acquisition, retention, and memory processing in SAMP8 mice Neurobiol Learn Mem 78 2002 125 138
140. W.A. Banks, S.A. Farr, J.E. Morley, K.M. Wolf, V. Geylis, and M. Steinitz Anti-amyloid beta protein antibody passage across the blood-brain barrier in the SAMP8 mouse model of Alzheimer's disease: an age-related selective uptake with reversal of learning impairment Exp Neurol 206 2007 248 256
141. W.A. Banks, B. Terrell, S.A. Farr, S.M. Robinson, N. Nonaka, and J.E. Morley Passage of amyloid beta protein antibody across the blood-brain barrier in a mouse model of Alzheimer's disease Peptides 23 2002 2223 2226
142. S.A. Farr, W.A. Banks, K. Uezu, A. Sano, F.S. Gaskin, and J.E. Morley Antibody to beta-amyloid protein increases acetylcholine in the hippocampus of 12 month SAP8 male mice Life Sci 73 2003 555 562
143. V.B. Kumar, K. Vyas, M. Franko, V. Choudhary, C. Buddhiraju, J. Alvarez, and et al. Molecular cloning, expression, and regulation of hippocampal amyloid precursor protein of senescence accelerated mouse (SAMP8) Biochem Cell Biol 79 2001 57 67
144. W.A. Banks, S.A. Farr, W. Butt, V.B. Kumar, M.W. Franko, and J.E. Morley Delivery across the blood-brain barrier of antisense directed against amyloid beta: reversal of learning and memory deficits in mice overexpressing amyloid precursor protein J Pharmacol Exp Ther 297 2001 1113 1121
145. H.F. Poon, G. Joshi, R. Sultana, S.A. Farr, W.A. Banks, J.E. Morley, and et al. Antisense directed at the Abeta region of APP decreases brain oxidative markers in aged senescence accelerated mice Brain Res 1018 2004 86 96
146. W.A. Banks, V.B. Kumar, S.A. Farr, R. Nakaoke, S.M. Robinson, and J.E. Morley Impairments in brain-to-blood transport of amyloid-β and reabsorption of cerebrospinal fluid in an animal model of Alzheimer's disease are reversed by antisense directed against amyloid-β protein precursor J Alzheimer Dis 23 2011 599 605
147. D. Dogrukol-Ak, V.B. Kumar, J.S. Ryerse, S.A. Farr, S. Verma, N. Nonaka, and et al. Isolation of peptide transport system-6 from brain endothelial cells: therapeutic effects with antisense inhibition in Alzheimer and stroke models J Cereb Blood Flow Metab 29 2009 411 422
148. S.A. Farr, M.A. Erickson, M.L. Niehoff, W.A. Banks, and J.E. Morley Central and peripheral administration of antisense oligonucleotide targeting amyloid-β protein precursor improves learning and memory and reduces neuroinflammatory cytokines in Tg2576 (AβPPswe) mice J Alzheimer Dis 40 2014 1005 1016