Skip to main content
Log in

Effect of quantity and quality of dietary protein on choline acetyltransferase and nerve growth factor, and their mRNAs in the cerebral cortex and hippocampus of rats

  • Original Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

The brain protein synthesis is sensitive to the dietary protein; however, the role of dietary protein on biomarkers including choline acetyltransferase and nerve growth factor (NGF) for the function of cholinergic neurons remains unknown in young rats. The purpose of this study was to determine whether the quantity and quality of dietary protein affects the concentration of NGF and activity of choline acetyltransferase, and their mRNA levels in the brains of young rats. Experiments were carried out on five groups of young rats (4 weeks) given the diets containing 0, 5, 20% casein, 20% gluten or 20% gelatin for 10 days. The activity of choline acetyltransferase in the cerebral cortex and hippocampus declined gradually with a decrease in quantity and quality of dietary protein. The concentration of NGF in the cerebral cortex and the mRNA levels of choline acetyltransferase in the cerebral cortex and hippocampus did not differ among groups. However, the concentration and mRNA level of NGF in the hippocampus was significantly lower in rats fed with lower quantity of protein or lower quality of protein. In the hippocampus, the mRNA levels of NGF significantly correlated with the NGF concentration when the quantity (r = 0.704, P < 0.01) and quality (r = 0.682, P < 0.01) of dietary protein was manipulated. It was further found that a significant positive correlation existed between the NGF concentration and the activity of choline acetyltransferase in the hippocampus (dietary protein quantity, r = 0.632, P < 0.05; dietary protein quality, r = 0.623, P < 0.05). These results suggest that the ingestion of lower quantity and quality of dietary protein are likely to control the mRNA level and concentration of NGF, and cause a decline in the activity of choline acetyltransferase in the brains of young rats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

NGF:

Nerve growth factor

GH:

Growth hormone

References

  • American Institute of Nutrition (1993) AIN purified diets for laboratory rodents: final report of the American Institute of Nutrition Ad Hoc Writing Committee on the reformulation of the AIN 76A rodent diet. J Nutr 123:1939–1951

    Google Scholar 

  • Appleyard ME, Smith AD, Wilcock GK, Esiri MM (1983) Decreased CSF acetylcholinesterase activity in Alzheimer’s disease. Lancet 2:452

    Article  PubMed  CAS  Google Scholar 

  • Ayger-LeLievre C, Olson L, Ebendal T, Seiger A, Persson H (1988) Expression of the beta-nerve growth factor gene in hippocampal neurons. Science 240:1339–1341

    Article  Google Scholar 

  • Burman P, Hetta J, Wide L, Mansson JE, Ekman R, Karlsson FA (1996) Growth hormone treatment affects brain neurotransmitters and thyroxine. Clin Endoclinol 44:319–324

    Article  CAS  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

  • Das TK, Waterlow JC (1974) The rate of adaptation of urea cycle enzymes in rat liver. Br J Nutr 32:353–373

    Article  PubMed  CAS  Google Scholar 

  • Deckwerth TL, Johnson EM Jr (1993) Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor. J Cell Biol 123:1207–1222

    Article  PubMed  CAS  Google Scholar 

  • Deijien JB, de Boer H, van der Veen EA (1998) Cognitive changes during growth hormone replacement in adult men. Psychoneuroendocrinology 23:45–55

    Article  Google Scholar 

  • Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42

    Article  Google Scholar 

  • Endo Y, Fu Z, Abe K, Arai S, Kato H (2002) Dietary protein quantity and quality affect rat hepatic gene expression. J Nutr 132:3632–3637

    PubMed  CAS  Google Scholar 

  • Fonnum F (1975) A rapid radiochemical method for the determination of choline acetyltransferase. J Neurochem 24:407–409

    Article  PubMed  CAS  Google Scholar 

  • Gibbs RB, Wu D, Hersh LB, Pfaff DW (1994) Effects of estrogen replacement on the relative levels of choline acetyltransferase, trk A and nerve growth factor messenger RNAs in the basal forebrain and hippocampal formation of adults rats. Exp Neurol 129:70–80

    Article  PubMed  CAS  Google Scholar 

  • Gibney J, Wallace JD, Spinks T, Schnorr L, Ranicar A, Cuneo RC, Lockhart S, Burnand KG, Salomon F, Sonksen PH, Russel-Jones D (1999) The effects of 10 years of recombinant human growth hormone (GH) in adult GH-deficient patients. J Clin Endoclinol Metab 84:2596–2602

    Article  CAS  Google Scholar 

  • Gnahn H, Hefti F, Heumann R, Schwab ME, Thoenen H (1983) NGF-mediated increase of choline acetyltransferase in the neonatal rat forebrain: evidence for a physiological role of NGF in the brain. Dev Brain Res 9:45–52

    Article  CAS  Google Scholar 

  • Hayase K, Tanaka M, Tujioka K, Hirano E, Habuchi O, Yokogoshi H (2001) 17-β-Estradiol affects brain protein synthesis rate in ovariectomized female rats. J Nutr 131:123–126

    PubMed  CAS  Google Scholar 

  • Hefti F (1986) Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. J Neurosci 6:2155–2162

    PubMed  CAS  Google Scholar 

  • Hefti F, Hartikka J, Knusel B (1989) Function of neurotrophic factors in the adult and aging brain and their possible use in the treatment of neurodegenerative diseases. Neurobiol Aging 10:515–533

    Article  PubMed  CAS  Google Scholar 

  • Imai S, Kanamoto R, Yagi I, Kotaru M, Saheki T, Iwami K (2003) Response of the induction of rat liver serine dehydratase to changes in the dietary protein requirement. Biosci Biotechnol Biochem 67:383–387

    Article  PubMed  CAS  Google Scholar 

  • Inestrosa NC, Perelman A (1990) Association of acetylcholinesterase with the cell surface. J Membr Biol 118:1–9

    Article  PubMed  CAS  Google Scholar 

  • Kato H, Kimura T (2003) Evaluation of the effects of the dietary intake of proteins and amino acids by DNA microarray technology. J Nutr 133:2073S–2077S

    PubMed  CAS  Google Scholar 

  • Korsching S, Auburger G, Heumann R, Scott J, Thoenen H (1985) Levels of nerve growth factor and its mRNA in the central nervous system of the rat correlate with cholinergic innervation. EMBO J 4:1389–1393

    PubMed  CAS  Google Scholar 

  • Kosik KS (1992) Alzheimer’s disease: a cell biological perspective. Science 256:780–783

    Article  PubMed  CAS  Google Scholar 

  • Lindsay RM, Wiegand SJ, Altar A, Distefano PS (1994) Neurotrophic factors: from molecule to man. Trends Neurosci 17:182–192

    Article  PubMed  CAS  Google Scholar 

  • Lyou S, Hirano E, Tujioka K, Mawatari Y, Hayase K, Okuyama S, Yokogoshi H (2002) Dietary genistein affects brain protein synthesis rates in ovariectomized female rats. J Nutr 132:2055–2058

    PubMed  CAS  Google Scholar 

  • Ohsumi M, Shi X, Tuchiya T, Tujioka K, Lyou S, Hayase K, Yokogoshi H (2007) The role of growth hormone and amino acids on brain protein synthesis in aged rats given proteins of different quantity and quality. Amino Acids 32(2):247–253

    Article  PubMed  CAS  Google Scholar 

  • Pan Y, Anthony M, Clarkson TB (1999) Effect of estradiol and soy phytoestrogens on choline acetyltransferase and nerve growth factor mRNAs in the frontal cortex and hippocampus of female rats. Proc Soc Exp Biol Med 221:118–125

    Article  PubMed  CAS  Google Scholar 

  • Reinstein DK, Isaacson RI, Dunn AJ (1979) Regional change in 2-deoxyglucose uptake after neocortical and hippocampal destruction. Brain Res 175:392–397

    Article  PubMed  CAS  Google Scholar 

  • Schimke RT (1962) Adaptive characteristics of urea cycle enzymes in the rat. J Biol Chem 237:459–468

    PubMed  CAS  Google Scholar 

  • Schneider-Rivas S, Rivas-Arancibia S, Vazquez-Pereyra F, Vezquez-Sandval R, Borgonio-Perez G (1995) Modulation of long-term memory and extinction responses induced by growth hormone (GH) and growth hormone releasing hormone (GHRH) in rats. Life Sci 56: PL433–PL441

    Article  PubMed  CAS  Google Scholar 

  • Schwab ME, Otten U, Agid Y, Thoenen H (1979) Nerve growth factor (NGF) in the rat CNS: absence of specific retrograde axonal transport and tyrosine hydroxylase induction in locus coeruleus and substantia nigra. Brain Res 168:473–483

    Article  PubMed  CAS  Google Scholar 

  • Seiler M, Schwab ME (1984) Specific retrograde transport of nerve growth factor (NGF) from neocortex to nucleus basalis in the rat. Brain Res 300:33–39

    Article  PubMed  CAS  Google Scholar 

  • Shelton DL, Reichardt LF (1986) Studies on the expression of the β-nerve growth factor (NGF) gene in the central nervous system: level and regional distribution of NGF mRNA suggest that NGF functions as a trophic factor for several distinct populations of neurons. Proc Natl Acad Sci USA 83:2714–2718

    Article  PubMed  CAS  Google Scholar 

  • Sherwin BB (1994) Estrogenic effects on memory in women. Ann N Y Acad Sci 743:213–231

    Article  PubMed  CAS  Google Scholar 

  • Singh M, Meyer EM, Millard WL, Simpkins JW (1994) Ovarian steroid deprovation results in a reversible learning impairment and compromised cholinergic function in female Sprague–Dawley rats. Brain Res 644:305–312

    Article  PubMed  CAS  Google Scholar 

  • Snedecor GW, Cochran WG (1967) Statistical methods, 6th edn. Iowa State University Press, Ames

    Google Scholar 

  • Steele RD, Harper AE (1990) Proteins and amino acids. In: Brown ML (eds) Present knowledge in nutrition, 6th edn. International Life Sciences Institute, Nutrition Foundation, Washington, DC, pp 333–340

    Google Scholar 

  • Tujioka K, Lyou S, Hirano E, Sano A, Hayase K, Yoshida A, Yokogoshi H (2002) Role of N-acetylglutamate concentration and ornithine transport into mitochondria in urea synthesis of rats given proteins of different quality. J Agric Food Chem 50:7467–7471

    Article  PubMed  CAS  Google Scholar 

  • Yokogoshi H, Hayase K, Yoshida A (1992) The quality and quantity of dietary protein affect brain protein synthesis in rats. J Nutr 122:2210–2217

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study is supported in part by a 21st Century COE program and city area promoting program from the Ministry of Education, Culture, Sports, Science and Technology, Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to K. Hayase.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tujioka, K., Shi, X., Ohsumi, M. et al. Effect of quantity and quality of dietary protein on choline acetyltransferase and nerve growth factor, and their mRNAs in the cerebral cortex and hippocampus of rats. Amino Acids 36, 13–19 (2009). https://doi.org/10.1007/s00726-007-0019-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-007-0019-0

Keywords

Navigation