A calorie-restricted diet decreases brain iron accumulation and preserves motor performance in old rhesus monkeys

Journal of Neuroscience

Volumn 30, Issue 23, 2010, Pages 7940-7947

  Kastman, Erik K ^a,b   Willette, Auriel A ^b,c   Coe, Christopher L ^c   Bendlin, Barbara B ^a,b   Kosmatka, Kris J ^a,b   McLaren, Donald G ^a,b,c   Xu, Guofan ^a,b   Canu, Elisa ^a,b   Field, Aaron S ^c   Alexander, Andrew L ^c   Voytko, Mary Lou ^d   Beasley, T Mark ^e   Colman, Ricki J ^e   Weindruch, Richard H ^a,b,f   Johnson, Sterling C ^a,b,c,f  

^a WILLIAM S MIDDLETON MEMORIAL VETERANS HOSPITAL   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d WAKE FOREST SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f UNIVERSITY OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IRON;

AGING; ARTICLE; ATTENUATION; BASAL GANGLION; BRAIN; BRAIN CORTEX; CALORIC RESTRICTION; CONTROLLED STUDY; FEMALE; GLOBUS PALLIDUS; IN VIVO STUDY; MALE; MOTOR PERFORMANCE; NEUROIMAGING; NEUROPROTECTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETAL LOBE; PRIORITY JOURNAL; RED NUCLEUS; RHESUS MONKEY; SUBSTANTIA NIGRA; TEMPORAL CORTEX; VELOCITY;

AGING; ANIMALS; BASAL GANGLIA; BRAIN; CALORIC RESTRICTION; FEMALE; GLOBUS PALLIDUS; IRON; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; MOTOR ACTIVITY; MOVEMENT; PARIETAL LOBE; RED NUCLEUS; SUBSTANTIA NIGRA; TEMPORAL LOBE;

EID: 77953520995     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0835-10.2010     Document Type: Article

References (80)

1. Anderson RM, Shanmuganayagam D, Weindruch R (2009) Caloric restriction and aging: studies in mice and monkeys. Toxicol Pathol 37:47-51.
2. Ansari MA, Scheff SW (2010) Oxidative stress in the progression of Alzheimer disease in the frontal cortex. J Neuropathol Exp Neurol 69:155-167.
3. Anson RM, Guo Z, de Cabo R, Iyun T, Rios M, Hagepanos A, Ingram DK, Lane MA, Mattson MP (2003) Intermittent fasting dissociates beneficial effects of dietary restriction on glucose metabolism and neuronal resistance to injury from calorie intake. Proc Natl Acad Sci U S A 100:6216-6220.
4. Ashburner J, Friston KJ (2000) Voxel-based morphometry: the methods. Neuroimage 11:805-821.
5. Bartzokis G, Beckson M, Hance DB, Marx P, Foster JA, Marder SR (1997) MR evaluation of age-related increase of brain iron in young adult and older normal males. Magn Reson Imaging 15:29-35.
6. Bartzokis G, Tishler TA, Lu PH, Villablanca P, Altshuler LL, Carter M, Huang D, Edwards N, Mintz J (2007) Brain ferritin iron may influence age- and gender-related risks of neurodegeneration. Neurobiol Aging 28:414-423.
7. Bishop GM, Smith MA, LaManna JC, Wilson AC, Perry G, Atwood CS (2007) Iron homeostasis is maintained in the brain, but not the liver, following mild hypoxia. Redox Rep 12:257-266.
8. Bizzi A, Brooks RA, Brunetti A, Hill JM, Alger JR, Miletich RS, Francavilla TL, Di Chiro G (1990) Role of iron and ferritin in MR imaging of the brain: a study in primates at different field strengths. Radiology 177:59-65.
9. Bradbury MW (1997) Transport of iron in the blood- brain- cerebrospinal fluid system. J Neurochem 69:443-454.
10. Brar S, Henderson D, Schenck J, Zimmerman EA (2009) Iron accumulation in the substantia nigra of patients with Alzheimer disease and Parkinsonism. Arch Neurol 66:371-374.
11. Calingasan NY, Gibson GE (2000) Dietary restriction attenuates the neuronal loss, induction of heme oxygenase-1 and blood- brain barrier breakdown induced by impaired oxidative metabolism. Brain Res 885:62-69.
12. Cass WA, Grondin R, Andersen AH, Zhang Z, Hardy PA, Hussey-Andersen LK, Rayens WS, Gerhardt GA, Gash DM (2007) Iron accumulation in the striatum predicts aging-related decline in motor function in rhesus monkeys. Neurobiol Aging 28:258-271.
13. Cattell RB (1966) The scree test for the number of factors. Multivariate Behaval Res 1:245-276.
14. Colman RJ, Beasley TM, Allison DB, Weindruch R (2008) Attenuation of sarcopenia by dietary restriction in rhesus monkeys. J Gerontol A Biol Sci Med Sci 63:556-559.
15. Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, Beasley TM, Allison DB, Cruzen C, Simmons HA, Kemnitz JW, Weindruch R (2009) Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325:201-204.
16. Dhenain M, Michot JL, Volk A, Picq JL, Boller F (1997) T2-weighted MRI studies of mouse lemurs: a primate model of brain aging. Neurobiol Aging 18:517-521.
17. Drayer B, Burger P, Darwin R, Riederer S, Herfkens R, Johnson GA (1986) MRI of brain iron. Am J Roentgenol 147:103-110.
18. Duan W, Mattson MP (1999) Dietary restriction and 2-deoxyglucose administration improve behavioral outcome and reduce degeneration of dopaminergic neurons in models of Parkinson's disease. J Neurosci Res 57:195-206.
19. Fontana L (2009) The scientific basis of caloric restriction leading to longer life. Curr Opin Gastroenterol 25:144-150.
20. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 33:636-647.
21. Forster MJ, Sohal BH, Sohal RS (2000) Reversible effects of long-term caloric restriction on protein oxidative damage. J Gerontol A Biol Sci Med Sci 55:B522-B529.
22. Gash DM, Zhang Z, Umberger G, Mahood K, Smith M, Smith C, Gerhardt GA (1999) An automated movement assessment panel for upper limb motor functions in rhesus monkeys and humans. J Neurosci Methods 89:111-117.
23. Gelman N, Gorell JM, Barker PB, Savage RM, Spickler EM, Windham JP, Knight RA (1999) MR imaging of human brain at 3.0 T: preliminary report on transverse relaxation rates and relation to estimated iron content. Radiology 210:759-767.
24. Grenier D, Pelletier D, Normandeau M, Newitt D, Nelson S, Goodkin DE, Majumdar S (2002) T2 relaxation time histograms in multiple sclerosis. Magn Reson Imaging 20:733-741.
25. Gorell JM, Ordidge RJ, Brown GG, Deniau JC, Buderer NM, Helpern JA (1995) Increased iron-related MRI contrast in the substantia nigra in Parkinson's disease. Neurology 45:1138-1143.
26. Gresl TA, Colman RJ, Roecker EB, Havighurst TC, Huang Z, Allison DB, Bergman RN, Kemnitz JW (2001) Dietary restriction and glucose regulation in aging rhesus monkeys: a follow-up report at 8.5 yr. Am J Physiol Endocrinol Metab 281:E757-E765.
27. Gresl TA, Colman RJ, Havighurst TC, Byerley LO, Allison DB, Schoeller DA, Kemnitz JW (2003) Insulin sensitivity and glucose effectiveness from three minimal models: effects of energy restriction and body fat in adult male rhesus monkeys. Am J Physiol Regul Integr Comp Physiol 285:R1340-R1354.
28. Grosser N, Oberle S, Berndt G, Erdmann K, Hemmerle A, Schröder H (2004) Antioxidant action of L-alanine: heme oxygenase-1 and ferritin as possible mediators. Biochem Biophys Res Commun 314:351-355.
29. Haacke EM, Cheng NY, House MJ, Liu Q, Neelavalli J, Ogg RJ, Khan A, Ayaz M, Kirsch W, Obenaus A (2005) Imaging iron stores in the brain using magnetic resonance imaging. Magn Reson Imaging 23:1-25.
30. Hallgren B, Sourander P (1958) The effect of age on the non-haemin iron in the human brain. J Neurochem 3:41-51.
31. Halliwell B, Gutteridge JM (1990) Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol 186:1-85.
32. Hardy PA, Gash D, Yokel R, Andersen A, Ai Y, Zhang Z (2005) Correlation of R2 with total iron concentration in the brains of rhesus monkeys. J Magn Reson Imaging 21:118-127.
33. Hayasaka S, Phan KL, Liberzon I, Worsley KJ, Nichols TE (2004) Nonstationary cluster-size inference with random field and permutation methods. Neuroimage 22:676-687.
34. Herndon JG, Moss MB, Rosene DL, Killiany RJ (1997) Patterns of cognitive decline in aged rhesus monkeys. Behav Brain Res 87:25-34.
35. House MJ, St Pierre TG, Kowdley KV, Montine T, Connor J, Beard J, Berger J, Siddaiah N, Shankland E, Jin LW (2007) Correlation of proton transverse relaxation rates (R2) with iron concentrations in postmortem brain tissue from Alzheimer's disease patients. Magn Reson Med 57:172-180.
36. Kayo T, Allison DB, Weindruch R, Prolla TA (2001) Influences of aging and caloric restriction on the transcriptional profile of skeletal muscle from rhesus monkeys. Proc Natl Acad Sci U S A 98:5093-5098.
37. Kemnitz JW, Weindruch R, Roecker EB, Crawford K, Kaufman PL, Ershler WB (1993) Dietary restriction of adult male rhesus monkeys: design, methodology, and preliminary findings from the first year of study. J Gerontol 48:B17-B26.
38. Koeppen AH (2003) A brief history of brain iron research. J Neurol Sci 207:95-97.
39. Lacreuse A, Herndon JG, Killiany RJ, Rosene DL, Moss MB (1999) Spatial cognition in rhesus monkeys: male superiority declines with age. Horm Behav 36:70-76.
40. Lovell MA, Ehmann WD, Butler SM, Markesbery WR (1995) Elevated thiobarbituric acid-reactive substances and antioxidant enzyme activity in the brain in Alzheimer's disease. Neurology 45:1594-1601.
41. Martin WR, Ye FQ, Allen PS (1998) Increasing striatal iron content associated with normal aging. Mov Disord 13:281-286.
42. Masoro EJ (2005) Overview of caloric restriction and ageing. Mech Ageing Dev 126:913-922.
43. Masoro EJ, McCarter RJ, Katz MS, McMahan CA (1992) Dietary restriction alters characteristics of glucose fuel use. J Gerontol 47:B202-B208.
44. Mastroberardino PG, Hoffman EK, Horowitz MP, Betarbet R, Taylor G, Cheng D, Na HM, Gutekunst CA, Gearing M, Trojanowski JQ, Anderson M, Chu CT, Peng J, Greenamyre JT (2009) A novel transferrin/TfR2-mediated mitochondrial iron transport system is disrupted in Parkinson's disease. Neurobiol Dis 34:417-431.
45. Maswood N, Young J, Tilmont E, Zhang Z, Gash DM, Gerhardt GA, Grondin R, Roth GS, Mattison J, Lane MA, Carson RE, Cohen RM, Mouton PR, Quigley C, Mattson MP, Ingram DK (2004) Caloric restriction increases neurotrophic factor levels and attenuates neurochemical and behavioral deficits in a primate model of Parkinson's disease. Proc Natl Acad Sci U S A 101:18171-18176.
46. Mattison JA, Roth GS, Lane MA, Ingram DK (2007) Dietary restriction in aging nonhuman primates. Interdiscip Top Gerontol 35:137-158.
47. McLaren DG, Kosmatka KJ, Oakes TR, Kroenke CD, Kohama SG, Matochik JA, Ingram DK, Johnson SC (2009) A population-average MRI-based atlas collection of the rhesus macaque. Neuroimage 45:52-59.
48. McLaren DG, Kosmatka KJ, Kastman EK, Bendlin BB, Johnson SC (2010) Rhesus macaque brain morphometry: a methodological comparison of voxel-wise approaches. Methods 50:157-165.
49. Mechelli A, Price CJ, Friston KJ, Ashburner J (2005) Voxel-based morphometry of the human brain: methods and applications. Curr Med Imaging Rev 1:105-113.
50. Moos T (2002) Brain iron homeostasis. Dan Med Bull 49:279-301.
51. Mouton PR, Chachich ME, Quigley C, Spangler E, Ingram DK (2009) Caloric restriction attenuates amyloid deposition in middle-aged dtg APP/ PS1 mice. Neurosci Lett 464:184-187.
52. Nagahara AH, Bernot T, Tuszynski MH (2010) Age-related cognitive deficits in rhesus monkeys mirror human deficits on an automated test battery. Neurobiol Aging 31:1020-1031.
53. Parker WD Jr, Parks J, Filley CM, Kleinschmidt-DeMasters BK (1994) Electron transport chain defects in Alzheimer's disease brain. Neurology 44:1090-1096.
54. Péran P, Hagberg G, Luccichenti G, Cherubini A, Brainovich V, Celsis P, Caltagirone C, Sabatini U (2007) Voxel-based analysis of R2* maps in the healthy human brain. J Magn Reson Imaging 26:1413-1420.
55. Poon CS, Henkelman RM (1992) Practical T2 quantitation for clinical applications. J Magn Reson Imaging 2:541-553.
56. Qin W, Yang T, Ho L, Zhao Z, Wang J, Chen L, Zhao W, Thiyagarajan M, MacGrogan D, Rodgers JT, Puigserver P, Sadoshima J, Deng H, Pedrini S, Gandy S, Sauve AA, Pasinetti GM (2006) Neuronal SIRT1 activation as a novel mechanism underlying the prevention of Alzheimer disease amyloid neuropathology by calorie restriction. J Biol Chem 281:21745-21754.
57. Raman A, Ramsey JJ, Kemnitz JW, Baum ST, Newton W, Colman RJ, Weindruch R, Beasley MT, Schoeller DA (2007) Influences of calorie restriction and age on energy expenditure in the rhesus monkey. Am J Physiol Endocrinol Metab 292:E101-E106.
58. Recalcati S, Invernizzi P, Arosio P, Cairo G (2008) New functions for an iron storage protein: the role of ferritin in immunity and autoimmunity. J Autoimmun 30:84-89.
59. Ribeiro LC, Quincozes-Santos A, Leite MC, Abib RT, Kleinkauf-Rocha J, Biasibetti R, Rotta LN, Wofchuk ST, Perry ML, Gonçalves CA, Gottfried C (2009) Caloric restriction increases hippocampal glutamate uptake and glutamine synthetase activity in Wistar rats. Neurosci Res 64:330-334.
60. Ridgway GR, Henley SM, Rohrer JD, Scahill RI, Warren JD, Fox NC (2008) Ten simple rules for reporting voxel-based morphometry studies. Neuroimage 40:1429-1435.
61. Roskams AJ, Connor JR (1990) Aluminum access to the brain: a role for transferrin and its receptor. Proc Natl Acad Sci U S A 87:9024-9027.
62. Saleem KS, Logothetis NK (2007) A combined MRI and histology atlas of the rhesus monkey brain in stereotaxic coordinates. London: Academic.
63. Schenck JF, Zimmerman EA (2004) High-field magnetic resonance imaging of brain iron: birth of a biomarker? NMR Biomed 17:433-445.
64. Stranahan AM, Lee K, Martin B, Maudsley S, Golden E, Cutler RG, Mattson MP (2009) Voluntary exercise and caloric restriction enhance hippocampal dendritic spine density and BDNF levels in diabetic mice. Hippocampus 19:951-961.
65. Tipton KF, Singer TP (1993) Advances in our understanding of the mechanisms of the neurotoxicity of MPTP and related compounds. J Neurochem 61:1191-1206.
66. Unger EL, Beard JL, Jones BC (2007) Iron regulation in C57BLI6 and DBA/2 mice subjected to iron overload. Nutr Neurosci 10:89-95.
67. Wanagat J, Allison DB, Weindruch R (1999) Caloric intake and aging: mechanisms in rodents and a study in nonhuman primates. Toxicol Sci 52:35-40.
68. Weindruch R, Walford RL (1988) The retardation of aging and disease by dietary restriction. Springfield, IL: Charles C. Thomas.
69. Willette AA, Bendlin BB, McLaren DG, Canu E, Kastman EK, Kosmatka KJ, Xu G, Field AS, Alexander AL, Colman RJ, Weindruch RH, Coe CL, Johnson SC (2010) Age-related changes in neural volume and microstructure associated with interleukin-6 are ameliorated by a calorie-restricted diet in old rhesus monkeys. Neuroimage 51:987-994.
70. Wilson AC, Clemente L, Liu T, Bowen RL, Meethal SV, Atwood CS (2008) Reproductive hormones regulate the selective permeability of the blood-brain barrier. Biochim Biophys Acta 1782:401-407.
71. Xu J, Knutson MD, Carter CS, Leeuwenburgh C (2008) Iron accumulation with age, oxidative stress and functional decline. PLoS One 3:e2865.
72. Xu X, Wang Q, Zhang M (2008) Age, gender, and hemispheric differences in iron deposition in the human brain: an in vivo MRI study. Neuroimage 40:35-42.
73. Yan SD, Chen X, Fu J, Chen M, Zhu H, Roher A, Slattery T, Zhao L, Nagashima M, Morser J, Migheli A, Nawroth P, Stern D, Schmidt AM (1996) RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 382:685-691.
74. Young IS, Woodside JV (2001) Antioxidants in health and disease. J Clin Pathol 54:176-186.
75. Zainal TA, Oberley TD, Allison DB, Szweda LI, Weindruch R (2000) Caloric restriction of rhesus monkeys lowers oxidative damage in skeletal muscle. FASEB J 14:1825-1836.
76. Zecca L, Gallorini M, Schünemann V, Trautwein AX, Gerlach M, Riederer P, Vezzoni P, Tampellini D (2001) Iron, neuromelanin and ferritin content in the substantia nigra of normal subjects at different ages: consequences for iron storage and neurodegenerative processes. J Neurochem 76:1766-1773.
77. Zecca L, Youdim MB, Riederer P, Connor JR, Crichton RR (2004a) Iron, brain ageing and neurodegenerative disorders. Nat Rev Neurosci 5:863-873.
78. Zecca L, Stroppolo A, Gatti A, Tampellini D, Toscani M, Gallorini M, Giaveri G, Arosio P, Santambrogio P, Fariello RG, Karatekin E, Kleinman MH, Turro N, Hornykiewicz O, Zucca FA (2004b) The role of iron and copper molecules in the neuronal vulnerability of locus coeruleus and substantia nigra during aging. Proc Natl Acad Sci U S A 101:9843-9848.
79. Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging 20:45-57.
80. Zhu WZ, Zhong WD, Wang W, Zhan CJ, Wang CY, Qi JP, Wang JZ, Lei T (2009) Quantitative MR phase-corrected imaging to investigate increased brain iron deposition of patients with Alzheimer disease. Radiology 253:497-504.