Blood withdrawal affects iron store dynamics in primates with consequences on monoaminergic system function

Neuroscience

Volumn 290, Issue , 2015, Pages 621-635

  Hyacinthe, C ^a,b   De Deurwaerdere, P ^a,b   Thiollier, T ^a,b,c   Li, Q ^d,e   Bezard, E ^a,b,d,e   Ghorayeb, I ^a,b,f  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b INSTITUT DES MALADIES NEURODÉGÉNÉRATIVES   (France)

^c Cynbiose   (France)

^d INSTITUTE OF LABORATORY ANIMAL SCIENCE   (China)

^e Williams House   (United Kingdom)

^f HÔPITAL PELLEGRIN   (France)

Author keywords

Dopamine; Ferritin; Iron; Non human primate; Restless legs syndrome Willis Ekbom disease; Serotonin

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 5 HYDROXYINDOLEACETIC ACID; DOPAMINE; FERRITIN; HEMOGLOBIN; HOMOVANILLIC ACID; LEVODOPA; MONOAMINE; NORADRENALIN; SEROTONIN; BIOGENIC AMINE; IRON;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE METABOLISM; FERRITIN BLOOD LEVEL; HEMOGLOBIN BLOOD LEVEL; IRON BLOOD LEVEL; IRON DEPLETION; IRON STORAGE; LOCOMOTION; MACACA FASCICULARIS; MALE; MONOAMINERGIC SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN CEREBROSPINAL FLUID LEVEL; TRANSFERRIN BLOOD LEVEL; ANIMAL; BLOOD; BLOOD ANALYSIS; BRAIN; CEREBROSPINAL FLUID; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; MICRODIALYSIS; MOTOR ACTIVITY; PHLEBOTOMY; PHYSIOLOGY; PUNCTURE;

ANIMALS; BIOGENIC MONOAMINES; BLOOD CHEMICAL ANALYSIS; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CIRCADIAN RHYTHM; IRON; MACACA FASCICULARIS; MALE; MICRODIALYSIS; MOTOR ACTIVITY; PHLEBOTOMY; SPINAL PUNCTURE;

EID: 84923163435     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.01.057     Document Type: Article

References (68)

1. Akpinar S. Restless legs syndrome treatment with dopaminergic drugs. Clin Neuropharmacol 1987, 10:69-79.
2. Aksu M., Bara-Jimenez W. State dependent excitability changes of spinal flexor reflex in patients with restless legs syndrome secondary to chronic renal failure. Sleep Med 2002, 3:427-430.
3. Allen R.P., Auerbach S., Bahrain H., Auerbach M., Earley C.J. The prevalence and impact of restless legs syndrome on patients with iron deficiency anemia. Am J Hematol 2013, 88:261-264.
4. Allen R.P., Picchietti D.L., Garcia-Borreguero D., Ondo W.G., Walters A.S., Winkelman J.W., Zucconi M., Ferri R., Trenkwalder C., Lee H.B., International Restless Legs Syndrome Study G Restless legs syndrome/Willis-Ekbom disease diagnostic criteria: updated International Restless Legs Syndrome Study Group (IRLSSG) consensus criteria - history, rationale, description, and significance. Sleep Med 2014, 15:860-873.
5. Ashkenazi R., Ben-Shachar D., Youdim M.B. Nutritional iron and dopamine binding sites in the rat brain. Pharmacol Biochem Behav 1982, 17(Suppl. 1):43-47.
6. Bara-Jimenez W., Aksu M., Graham B., Sato S., Hallett M. Periodic limb movements in sleep: state-dependent excitability of the spinal flexor reflex. Neurology 2000, 54:1609-1616.
7. Barraud Q., Obeid I., Aubert I., Barriere G., Contamin H., McGuire S., Ravenscroft P., Porras G., Tison F., Bezard E., Ghorayeb I. Neuroanatomical study of the A11 diencephalospinal pathway in the non-human primate. PLoS ONE 2010, 5:e13306.
8. Baumgartner J., Smuts C.M., Malan L., Arnold M., Yee B.K., Bianco L.E., Boekschoten M.V., Muller M., Langhans W., Hurrell R.F., Zimmermann M.B. Combined deficiency of iron and (n-3) fatty acids in male rats disrupts brain monoamine metabolism and produces greater memory deficits than iron deficiency or (n-3) fatty acid deficiency alone. J Nutr 2012, 142:1463-1471.
9. Beard J.L., Chen Q., Connor J., Jones B.C. Altered monamine metabolism in caudate-putamen of iron-deficient rats. Pharmacol Biochem Behav 1994, 48:621-624.
10. Ben-Shachar D., Ashkenazi R., Youdim M.B. Long-term consequence of early iron-deficiency on dopaminergic neurotransmission in rats. Int J Dev Neurosci 1986, 4:81-88.
11. Ben-Shachar D., Finberg J.P., Youdim M.B. Effect of iron chelators on dopamine D2 receptors. J Neurochem 1985, 45:999-1005.
12. Bianco L.E., Unger E.L., Earley C.J., Beard J.L. Iron deficiency alters the day-night variation in monoamine levels in mice. Chronobiol Int 2009, 26:447-463.
13. Bianco L.E., Wiesinger J., Earley C.J., Jones B.C., Beard J.L. Iron deficiency alters dopamine uptake and response to L-DOPA injection in Sprague-Dawley rats. J Neurochem 2008, 106:205-215.
14. Burdo J.R., Connor J.R. Brain iron uptake and homeostatic mechanisms: an overview. Biometals 2003, 16:63-75.
15. Burhans M.S., Dailey C., Beard Z., Wiesinger J., Murray-Kolb L., Jones B.C., Beard J.L. Iron deficiency: differential effects on monoamine transporters. Nutr Neurosci 2005, 8:31-38.
16. Camus S.M., Blois-Heulin C., Li Q., Hausberger M., Bezard E. Behavioural profiles in captive-bred cynomolgus macaques: towards monkey models of mental disorders?. PLoS One 2013, 8:e62141.
17. Chen Q.B., Beard J.L., Jones B.C. Abnormal rat brain monoamine metabolism in iron deficiency anemia. J Nutr Biochem 1995, 6:486-493.
18. Connor J.R., Boyer P.J., Menzies S.L., Dellinger B., Allen R.P., Ondo W.G., Earley C.J. Neuropathological examination suggests impaired brain iron acquisition in restless legs syndrome. Neurology 2003, 61:304-309.
19. Connor J.R., Wang X.S., Allen R.P., Beard J.L., Wiesinger J.A., Felt B.T., Earley C.J. Altered dopaminergic profile in the putamen and substantia nigra in restless leg syndrome. Brain 2009, 132:2403-2412.
20. Connor J.R., Wang X.S., Patton S.M., Menzies S.L., Troncoso J.C., Earley C.J., Allen R.P. Decreased transferrin receptor expression by neuromelanin cells in restless legs syndrome. Neurology 2004, 62:1563-1567.
21. De Deurwaerdere P., Bonhomme N., Le Moal M., Spampinato U. D-fenfluramine increases striatal extracellular dopamine in vivo independently of serotonergic terminals or dopamine uptake sites. J Neurochem 1995, 65:1100-1108.
22. Diehl K.H., Hull R., Morton D., Pfister R., Rabemampianina Y., Smith D., Vidal J.M., van de Vorstenbosch C. A good practice guide to the administration of substances and removal of blood, including routes and volumes. J Appl Toxicol 2001, 21:15-23.
23. Earley C.J., Connor J., Garcia-Borreguero D., Jenner P., Winkelman J., Zee P.C., Allen R. Altered Brain iron homeostasis and dopaminergic function in restless legs syndrome (Willis-Ekbom disease). Sleep Med 2014, 15(11):1288-1301.
24. Earley C.J., Connor J.R., Beard J.L., Malecki E.A., Epstein D.K., Allen R.P. Abnormalities in CSF concentrations of ferritin and transferrin in restless legs syndrome. Neurology 2000, 54:1698-1700.
25. Earley C.J., Kuwabara H., Wong D.F., Gamaldo C., Salas R., Brasic J., Ravert H.T., Dannals R.F., Allen R.P. The dopamine transporter is decreased in the striatum of subjects with restless legs syndrome. Sleep 2011, 34:341-347.
26. Earley C.J., Kuwabara H., Wong D.F., Gamaldo C., Salas R.E., Brasic J.R., Ravert H.T., Dannals R.F., Allen R.P. Increased synaptic dopamine in the putamen in restless legs syndrome. Sleep 2013, 36:51-57.
27. Engeln M., De Deurwaerdere P., Li Q., Bezard E., Fernagut P.O. Widespread monoaminergic dysregulation of both motor and non-motor circuits in parkinsonism and dyskinesia. Cereb Cortex 2014, Apr 25. [Epub ahead of print].
28. Erikson K.M., Jones B.C., Beard J.L. Iron deficiency alters dopamine transporter functioning in rat striatum. J Nutr 2000, 130:2831-2837.
29. Erikson K.M., Jones B.C., Hess E.J., Zhang Q., Beard J.L. Iron deficiency decreases dopamine D1 and D2 receptors in rat brain. Pharmacol Biochem Behav 2001, 69:409-418.
30. Erikson K.M., Pinero D.J., Connor J.R., Beard J.L. Regional brain iron, ferritin and transferrin concentrations during iron deficiency and iron repletion in developing rats. J Nutr 1997, 127:2030-2038.
31. Fernagut P.O., Li Q., Dovero S., Chan P., Wu T., Ravenscroft P., Hill M., Chen Z., Bezard E. Dopamine transporter binding is unaffected by L-DOPA administration in normal and MPTP-treated monkeys. PLoS One 2010, 5:e14053.
32. Fitoussi A., Dellu-Hagedorn F., De Deurwaerdere P. Monoamines tissue content analysis reveals restricted and site-specific correlations in brain regions involved in cognition. Neuroscience 2013, 255:233-245.
33. Fitzpatrick P.F. Tetrahydropterin-dependent amino acid hydroxylases. Annu Rev Biochem 1999, 68:355-381.
34. Glover J., Jacobs A. Activity pattern of iron-deficient rats. Br Med J 1972, 2:627-628.
35. Hemmeler G. Métabolisme du fer. Physiologie - pathologie - traitement 1951, Masson & Cie, Paris. P. Masson (Ed.).
36. Hening W., Allen R., Earley C., Kushida C., Picchietti D., Silber M. The treatment of restless legs syndrome and periodic limb movement disorder. An American Academy of Sleep Medicine Review. Sleep 1999, 22:970-999.
37. Hensler J.G., Artigas F., Bortolozzi A., Daws L.C., De Deurwaerdere P., Milan L., Navailles S., Koek W. Catecholamine/Serotonin interactions: systems thinking for brain function and disease. Adv Pharmacol 2013, 68:167-197.
38. Hentze M.W., Muckenthaler M.U., Galy B., Camaschella C. Two to tango: regulation of mammalian iron metabolism. Cell 2010, 142:24-38.
39. Jhoo J.H., Yoon I.Y., Kim Y.K., Chung S., Kim J.M., Lee S.B., Kim T.H., Moon S.H., Kim S.E., Kim K.W. Availability of brain serotonin transporters in patients with restless legs syndrome. Neurology 2010, 74:513-518.
40. Kasparov S., Teschemacher A.G. Altered central catecholaminergic transmission and cardiovascular disease. Exp Physiol 2008, 93:725-740.
41. Kuhn E., Brodan V. Changes in the circadian rhythm of serum iron induced by a 5-day sleep deprivation. Eur J Appl Physiol Occup Physiol 1982, 49:215-222.
42. LeVine S.M., Wulser M.J., Lynch S.G. Iron quantification in cerebrospinal fluid. Anal Biochem 1998, 265:74-78.
43. Martin R.F., Bowden D.M. A stereotaxic template atlas of the macaque brain for digital imaging and quantitative neuroanatomy. NeuroImage 1996, 4:119-150.
44. Mizuno S., Mihara T., Miyaoka T., Inagaki T., Horiguchi J. CSF iron, ferritin and transferrin levels in restless legs syndrome. J Sleep Res 2005, 14:43-47.
45. Navailles S., Benazzouz A., Bioulac B., Gross C., De Deurwaerdere P. High-frequency stimulation of the subthalamic nucleus and L-3,4-dihydroxyphenylalanine inhibit in vivo serotonin release in the prefrontal cortex and hippocampus in a rat model of Parkinson's disease. J Neurosci 2010, 30:2356-2364.
46. Navailles S., De Deurwaerdere P. Presynaptic control of serotonin on striatal dopamine function. Psychopharmacology 2011, 213:213-242.
47. Nelson C., Erikson K., Pinero D.J., Beard J.L. In vivo dopamine metabolism is altered in iron-deficient anemic rats. J Nutr 1997, 127:2282-2288.
48. O'Keeffe S.T., Gavin K., Lavan J.N. Iron status and restless legs syndrome in the elderly. Age Ageing 1994, 23:200-203.
49. Ondo W.G., He Y., Rajasekaran S., Le W.D. Clinical correlates of 6-hydroxydopamine injections into A11 dopaminergic neurons in rats: a possible model for restless legs syndrome. Mov Disord 2000, 15:154-158.
50. Pappas S.S., Behrouz B., Janis K.L., Goudreau J.L., Lookingland K.J. Lack of D2 receptor mediated regulation of dopamine synthesis in A11 diencephalospinal neurons in male and female mice. Brain Res 2008, 1214:1-10.
51. Pittock S.J., Parrett T., Adler C.H., Parisi J.E., Dickson D.W., Ahlskog J.E. Neuropathology of primary restless leg syndrome: absence of specific τ- and α-synuclein pathology. Mov Disord 2004, 19:695-699.
52. Porras G., De Deurwaerdere P., Li Q., Marti M., Morgenstern R., Sohr R., Bezard E., Morari M., Meissner W.G. L-dopa-induced dyskinesia: beyond an excessive dopamine tone in the striatum. Sci Rep 2014, 4:3730.
53. Qu S., Le W., Zhang X., Xie W., Zhang A., Ondo W.G. Locomotion is increased in a11-lesioned mice with iron deprivation: a possible animal model for restless legs syndrome. J Neuropathol Exp Neurol 2007, 66:383-388.
54. Ramsey A.J., Fitzpatrick P.F. Effects of phosphorylation of serine 40 of tyrosine hydroxylase on binding of catecholamines: evidence for a novel regulatory mechanism. Biochemistry 1998, 37:8980-8986.
55. Ramsey A.J., Hillas P.J., Fitzpatrick P.F. Characterization of the active site iron in tyrosine hydroxylase. Redox states of the iron. J Biol Chem 1996, 271:24395-24400.
56. Rao R., Ennis K., Oz G., Lubach G.R., Georgieff M.K., Coe C.L. Metabolomic analysis of cerebrospinal fluid indicates iron deficiency compromises cerebral energy metabolism in the infant monkey. Neurochem Res 2013, 38:573-580.
57. Rottach K.G., Schaner B.M., Kirch M.H., Zivotofsky A.Z., Teufel L.M., Gallwitz T., Messer T. Restless legs syndrome as side effect of second generation antidepressants. J Psychiatr Res 2008, 43:70-75.
58. Severson C.A., Wang W., Pieribone V.A., Dohle C.I., Richerson G.B. Midbrain serotonergic neurons are central pH chemoreceptors. Nat Neurosci 2003, 6:1139-1140.
59. Third J.L., Ryan M.D., Sothern R.B., Dawson S., McCormick J.B., Hoffman H.S., Gathing A., Jankowski R.A., Kania K.S., Kanabrocki E.L. Circadian distribution of iron and ferritin in serum of healthy and type 2 diabetic males. Clin Ter 2006, 157:35-40.
60. Unger E.L., Bianco L.E., Jones B.C., Allen R.P., Earley C.J. Low brain iron effects and reversibility on striatal dopamine dynamics. Exp Neurol 2014, 261C:462-468.
61. Unger E.L., Paul T., Murray-Kolb L.E., Felt B., Jones B.C., Beard J.L. Early iron deficiency alters sensorimotor development and brain monoamines in rats. J Nutr 2007, 137:118-124.
62. Wadsworth G.R. Haemoglobin levels of normal men and women living in a tropical climate. Br Med J 1954, 2:910-911.
63. Westerink B.H., Damsma G., De Vries J.B., Koning H. Dopamine re-uptake inhibitors show inconsistent effects on the in vivo release of dopamine as measured by intracerebral dialysis in the rat. Eur J Pharmacol 1987, 135:123-128.
64. Westerink B.H., Van Putten F.M. Simultaneous determination of the rates of synthesis and metabolism of dopamine in various areas of the rat brain: application to the effects of (+)-amphetamine. Eur J Pharmacol 1987, 133:103-110.
65. Wills L., Stewart A. Experimental anaemia in monkeys, with special reference to macrocytic nutritional anaemia. Br J Exp Pathol 1935, 16:444-453.
66. Youdim M.B., Ben-Shachar D., Yehuda S. Putative biological mechanisms of the effect of iron deficiency on brain biochemistry and behavior. Am J Clin Nutr 1989, 50:607-615. discussion 607-615.
67. Zhao H., Zhu W., Pan T., Xie W., Zhang A., Ondo W.G., Le W. Spinal cord dopamine receptor expression and function in mice with 6-OHDA lesion of the A11 nucleus and dietary iron deprivation. J Neurosci Res 2007, 85:1065-1076.
68. Zwart A. Spectrophotometry of hemoglobin: various perspectives. Clin Chem 1993, 39:1570-1572.