Differential effects of low-phenylalanine protein sources on brain neurotransmitters and behavior in C57Bl/6-Pahenu2 mice

Molecular Genetics and Metabolism

Volumn 111, Issue 4, 2014, Pages 452-461

  Sawin, Emily A ^a   Murali, Sangita G ^a   Ney, Denise M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Catecholamines; Glycomacropeptide; Marble burying; Open field; Phenylketonuria; Serotonin

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; ADRENALIN; CASEIN; CATECHOLAMINE; DOPAMINE; GLYCOPROTEIN; HISTIDINE; HOMOVANILLIC ACID; ISOLEUCINE; LEUCINE; NEUROTRANSMITTER; NORADRENALIN; PHENYLALANINE; SEROTONIN; THREONINE; TRYPTOPHAN; TYROSINE; VALINE; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CASEINOMACROPEPTIDE; PEPTIDE FRAGMENT; PROTEIN INTAKE;

AMINO ACID BLOOD LEVEL; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN WEIGHT; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOARCHITECTURE; DOPAMINE METABOLISM; ELECTROCHEMICAL DETECTION; EXPLORATORY BEHAVIOR; FEMALE; GENOTYPE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYPERACTIVITY; LOCOMOTION; MALE; MARBLE BURYING TEST; MOBILIZATION; MOUSE; NONHUMAN; OPEN FIELD TEST; PHENOTYPE; PHENYLKETONURIA; PRIORITY JOURNAL; SEROTONIN BRAIN LEVEL; SEX; WILD TYPE; ANIMAL; BLOOD; BRAIN; C57BL MOUSE; DRUG EFFECTS; METABOLISM; MOTOR ACTIVITY; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; PHARMACOLOGY; PROTEIN INTAKE; TIME;

MUS;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CASEINS; CATECHOLAMINES; DIETARY PROTEINS; FEMALE; GENOTYPE; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; NEUROTRANSMITTER AGENTS; ORGAN SIZE; PEPTIDE FRAGMENTS; PHENYLALANINE; PHENYLKETONURIAS; SEROTONIN; TIME FACTORS;

EID: 84897573768     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2014.01.015     Document Type: Article

References (65)

1. National Institutes of Health Phenylketonuria (PKU): screening and management. NIH consensus statement 2000, 17 no. 3:1-33.
2. MacLeod Erin L., Ney Denise M. Nutritional management of phenylketonuria. Ann. Nestle (English ed.) 2010, 68:58-69.
3. De Groot M.J., Hoeksma M., Blau N., Reijngoud D.J., Van Spronsen F.J. Pathogenesis of cognitive dysfunction in phenylketonuria: review of hypotheses. Mol. Genet. Metab. 2010, 99:S86-S89.
4. Azadi B., Seddigh A., Tehrani-Doost M., Alaghband-Rad J., Ashrafi M.R. Executive dysfunction in treated phenylketonuric patients. Eur. Child Adolesc. Psychiatry 2009, 18:360-368.
5. Christ S.E., Huijbregts S.C., de Sonneville L.M., White D.A. Executive function in early-treated phenylketonuria: profile and underlying mechanisms. Mol. Genet. Metab. 2010, 99:S22-S32.
6. Landvogt C., Mengel E., Bartenstein P., Buchholz H.G., Schreckenberger M., Siessmeier T., Scheurich A., Feldmann R., Weglage J., Cumming P., Zepp F., Ullrich K. Reduced cerebral fluoro-l-dopamine uptake in adult patients suffering from phenylketonuria. J. Cereb. Blood Flow Metab. 2007, 28:824-831.
7. Güttler F., Lou H. Dietary problems of phenylketonuria: effect on CNS transmitters and their possible role in behaviour and neuropsychological function. J. Inherit. Metab. Dis. 1986, 9:169-177.
8. Pascucci T., Ventura R., Puglisi-Allegra S., Cabib S. Deficits in brain serotonin synthesis in a genetic mouse model of phenylketonuria. Neuroreport 2002, 13:2561-2564.
9. Pardridge W.M. Blood-brain barrier carrier-mediated transport and brain metabolism of amino acids. Neurochem. Res. 1998, 23:635-644.
10. McKean C.M. The effects of high phenylalanine concentrations on serotonin and catecholamine metabolism in the human brain. Brain Res. 1972, 47:469-476.
11. Pare C.M.B., Sandler M., Stacey R.S. Decreased 5-hydroxytryptophan decarboxylase activity in phenylketonuria. Lancet 1958, 272:1099-1101.
12. Sandler M. Inborn errors and disturbances of central neurotransmission (with special reference to phenylketonuria). J. Inherit. Metab. Dis. 1982, 5:65-70.
13. Shedlovsky A., McDonald J.D., Symula D., Dove W.F. Mouse models of human phenylketonuria. Genetics 1993, 134:1205-1210.
14. McDonald J.D., Charlton C.K. Characterization of mutations at the mouse phenylalanine hydroxylase locus. Genomics 1997, 39:402-405.
15. Puglisi-Allegra S., Cabib S., Pascucci T., Ventura R., Cali F., Romano V. Dramatic brain aminergic deficit in a genetic mouse model of phenylketonuria. Neuroreport 2000, 11:1361-1364.
16. Pascucci T., Andolina D., Ventura R., Puglisi-Allegra S., Cabib S. Reduced availability of brain amines during critical phases of postnatal development in a genetic mouse model of cognitive delay. Brain Res. 2008, 1217:232-238.
17. Sarkissian C.N., Boulais D.M., McDonald J.D., Scriver C.R. A heteroallelic mutant mouse model: a new orthologue for human hyperphenylalaninemia. Mol. Genet. Metab. 2000, 69:188-194.
18. Mihalick S.M., Langlois J.C., Krienke J.D., Dube W.V. An olfactory discrimination procedure for mice. J. Exp. Anal. Behav. 2000, 73:305-318.
19. Cabib S., Pascucci T., Ventura R., Romano V., Puglisi-Allegra S. The behavioral profile of severe mental retardation in a genetic mouse model of phenylketonuria. Behav. Genet. 2003, 33:301-310.
20. Martynyuk A.E., Van Spronsen F.J., Van der Zee E.A. Animal models of brain dysfunction in phenylketonuria. Mol. Genet. Metab. 2010, 99:S100-S105.
21. Ding Z., Georgiev P., Thöny B. Administration-route and gender-independent long-term therapeutic correction of phenylketonuria (PKU) in a mouse model by recombinant adeno-associated virus 8 pseudotyped vector-mediated gene transfer. Gene Ther. 2005, 13:587-593.
22. Koch R., Burton B., Hoganson G., Peterson R., Rhead W., Rouse B., Scott R., et al. Phenylketonuria in adulthood: a collaborative study. J. Inherit. Metab. Dis. 2002, 25:333-346.
23. MacDonald A. Diet and compliance in phenylketonuria. Eur. J. Pediatr. 2000, 159:S136-S141.
24. MacDonald A., Daly A., Davies P., Asplin D., Hall S.K., Rylance G., Chakrapani A. Protein substitutes for PKU: What's new?. J. Inherit. Metab. Dis. 2004, 27:363-371.
25. Walter J.Η., White F.J. Blood phenylalanine control in adolescents with phenylketonuria. Int. J. Adolesc. Med. Health 2004, 16:41-46.
26. Enns G.M., Koch R., Brumm V., Blakely E., Suter R., Jurecki E. Suboptimal outcomes in patients with PKU treated early with diet alone: revisiting the evidence. Mol. Genet. Metab. 2010, 101:99-109.
27. Nielsen J.B. Effect of dietary tryptophan supplement on neurotransmitter metabolism in phenylketonuria. Dietary phenylalanine and brain function 1988, 261-264. Birkhäuser Boston.
28. Lykkelund C., Nielsen J.B., Lou H.C., Rasmussen V., Gerdes A.M., Christensen E., Güttler F. Increased neurotransmitter biosynthesis in phenylketonuria induced by phenylalanine restriction or by supplementation of unrestricted diet with large amounts of tyrosine. Eur. J. Pediatr. 1988, 148:238-245.
29. Yano S., Moseley K., Azen C. Large neutral amino acid supplementation increases melatonin synthesis in phenylketonuria: a new biomarker. J. Pediatr. 2013, 162:999-1003.
30. Etzel M.R. Manufacture and use of dairy protein fraction. J. Nutr. 2004, 134:996S-1002S.
31. Ney D.M., Gleason S.T., Van Calcar S.C., MacLeod E.L., Nelson K.L., Etzel M.R., Rice G.M., Wolff J.A. Nutritional management of PKU with glycomacropeptide from cheese whey. J. Inherit. Metab. Dis. 2009, 32:32-39.
32. van Calcar S.C., MacLeod E.L., Gleason S.T., Etzel M.R., Clayton M.K., Wolff J.A., Ney D.M. Improved nutritional management of phenylketonuria by using a diet containing glycomacropeptide compared with amino acids. Am. J. Clin. Nutr. 2009, 89:1068-1077.
33. Ney D.M., Hull A.K., van Calcar S.C., Liu X., Etzel M.R. Dietary glycomacropeptide supports growth and reduces the concentrations of phenylalanine in plasma and brain in a murine model of phenylketonuria. J. Nutr. 2008, 138:316-322.
34. McDonald J.D., Bode V.C., Dove W.F., Shedlovsky A. Pahhph-5: a mouse mutant deficient in phenylalanine hydroxylase. Proc. Natl. Acad. Sci. 1990, 87:1965-1967.
35. Harding C.O., Gillingham M.B., Hamman K., Clark H., Goebel-Daghighi E., Bird A., Koeberl D.D. Complete correction of hyperphenylalanemia following liver-directed, recombinant AAV2/8 vector-mediated gene therapy in murine phenylketonuria. Gene Ther 2006, 13:457-462.
36. Solverson P., Murali S.G., Brinkman A.S., Nelson D.W., Clayton M.K., Yen Chi-Liang E., Ney D.M. Glycomacropeptide, a low-phenylalanine protein isolated from cheese whey, supports growth and attenuates metabolic stress in the murine model of phenylketonuria. Am. J. Physiol. Endocrinol. Metab. 2012, 302:E885-E895.
37. Rogers Q.R., Harper A.E. Amino acid diets and maximal growth in the rat. J. Nutr. 1965, 87:267-273.
38. Slocum R.H., Cummings J.G. "Amino acid analysis of physiological samples." Techniques in diagnostic human biochemical genetics: a laboratory manual 1991, 87-126. Wiley-Liss, New York.
39. McCall M.A., Gregg R.G., Behringer R.R., Brenner M., Delaney C.L., Galbreath E.J., Zhang C.L., Pearce R.A., Chiu S.Y., Messing A. Targeted deletion in astrocyte intermediate filament (Gfap) alters neuronal physiology. Proc. Natl. Acad. Sci. 1996, 93:6361-6366.
40. Thomas A., Burant A., Bui N., Graham D., Yuva-Paylor L.A., Paylor R. Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety. Psychopharmacology 2009, 204:361-373.
41. Deacon R.M.J. Digging and marble burying in mice: simple methods for in vivo identification of biological impacts. Nat. Protoc. 2006, 1:122-124.
42. Holmes A., Wrenn C.C., Harris A.P., Thayer K.E., Crawley J.N. Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice, Genes. Brain Behav. 2002, 1:55-69.
43. 4 receptor modulates analgesic response and acoustic startle response in a mouse model of fragile X syndrome (FXS). Behav. Brain Res. 2012, 228:1-8.
44. Berg R.M., Taudorf S., Bailey D.M., Lundby C., Larsen F.S., Pedersen B.K., Møller K. Cerebral net exchange of large neutral amino acids after lipopolysaccharide infusion in healthy humans. Crit. Care 2010, 14:R16.
45. Dobkin C., Rabe A., Dumas R., Idrissi A.E., Haubenstock H., Brown W.T. Fmr 1 knockout mouse has a distinctive strain-specific learning impairment. Neuroscience 2000, 100:423-429.
46. Bickel H., Gerrard J., Hickmans E.M. Influence of phenylalanine intake on phenylketonuria. Lancet 1953, 265:812.
47. Bickel H., Gerrard J., Hickmans E.M. The influence of phenylalanine intake on the chemistry and behaviour of a phenylketonuria child. Acta Paediatr. 1954, 43:64-77.
48. Mochizuki S., Mizukami H., Ogura T., Kure S., Ichinohe A., Kojima K., Matsubara Y., et al. Long-term correction of hyperphenylalaninemia by AAV-mediated gene transfer leads to behavioral recovery in phenylketonuria mice. Gene Ther. 2004, 11:1081-1086.
49. Yannicelli S., Ryan A. Improvements in behaviour and physical manifestations in previously untreated adults with phenylketonuria using a phenylalanine-restricted diet: a national survey. J. Inherit. Metab. Dis. 1995, 18:131-134.
50. Arnold G.L., Vladutiu C.J., Orlowski C.C., Blakely E.M., DeLuca J. Prevalence of stimulant use for attentional dysfunction in children with phenylketonuria. J. Inherit. Metab. Dis. 2004, 27:137-143.
51. Russell V., de Villiers A., Sagvolden T., Lamm M., Taljaard J. Altered dopaminergic function in the prefrontal cortex, nucleus accumbens and caudate-putamen of an animal model of attention-deficit hyperactivity disorder-the spontaneously hypertensive rat. Brain Res. 1995, 676:343-351.
52. Bymaster F.P., Katner J.S., Nelson D.L., Hemrick-Luecke S.K., Threlkeld P.G., Heiligenstein J.H., Morin S.M., Gehlert D.R., Perry K.W. Atomoxetine increases extracellular levels of norepinephrine and dopamine in prefrontal cortex of rat: a potential mechanism for efficacy in attention deficit/hyperactivity disorder. Neuropsychopharmacology 2002, 27:699-711.
53. Stevenson M., McNaughton N. A comparison of phenylketonuria with attention deficit hyperactivity disorder: do markedly different aetiologies deliver common phenotypes?. Brain Res. Bull. 2013, 99:63-83.
54. Heikkinen T., Puoliväli J., Liu L., Rissanen A., Tanila H. Effects of ovariectomy and estrogen treatment on learning and hippocampal neurotransmitters in mice. Horm. Behav. 2002, 41:22-32.
55. Luine V.N., Richards S.T., Wu V.Y., Beck K.D. Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Horm. Behav. 1998, 34:149-162.
56. Vries G.J. Sex differences in neurotransmitter systems. J. Neuroendocrinol. 1990, 2:1-13.
57. 1A receptor binding potential measured by PET using [C-11] WAY-100635. Brain Res. 2002, 954:173-182.
58. Stemerdink B.A., Kalverboer A.F., Van der Meere J.J., Van der Molen M.W., Huisman J., de Jong L.W.A., Slijper F.M.E., Verkerk P.H., van Spronsen F.J. Behaviour and school achievement in patients with early and continuously treated phenylketonuria. J. Inherit. Metab. Dis. 2000, 23:548-562.
59. Cases O., Seif I., Grimsby J., Gaspar P., Chen K., Pournin S., Müller U., et al. Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 1995, 268:1763.
60. Gerson S.C., Baldessarini R.J. Motor effects of serotonin in the central nervous system. Life Sci. 1980, 27:1435-1451.
61. Newell D.W., Barth A., Ricciardi T.N., Malouf A.T. Glycine causes increased excitability and neurotoxicity by activation of NMDA receptors in the hippocampus. Exp. Neurol. 1997, 145:235-244.
62. Lipina T., Labrie V., Weiner I., Roder J. Modulators of the glycine site on NMDA receptors, d-serine and ALX 5407, display similar beneficial effects to clozapine in mouse models of schizophrenia. Psychopharmacology 2005, 179:54-67.
63. McMahon, R. J., B. Wang, J. Brand-Miller, and S. C. Rumsey, method of improving learning and memory in mammals, WIPO patent 2006118719, issued November 10, 2006.
64. Scholtz S.A., Gottipati B.S., Gajewski B.J., Carlson S.E. Dietary sialic acid and cholesterol influence cortical composition in developing rats. J. Nutr. 2013, 143:132-135.
65. Wang B., Yu B., Karim M., Hu H., Sun Y., McGreevy P., Petocz P., Held S., Brand-Miller J. Dietary sialic acid supplementation improves learning and memory in piglets. Am. J. Clin. Nutr. 2007, 85:561-569.