Branched-chain amino acids influence the immune properties of microglial cells and their responsiveness to pro-inflammatory signals

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 5, 2013, Pages 650-659

  De Simone, Roberta ^a   Vissicchio, Federica ^a   Mingarelli, Cecilia ^a   De Nuccio, Chiara ^a   Visentin, Sergio ^a   Ajmone Cat, Maria Antonietta ^a   Minghetti, Luisa ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

BCAA; Brain macrophages; M1 phenotype; M2 phenotype; Microglial activation; Neurodegeneration

Indexed keywords

AMINO ACID; INTERLEUKIN 10;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN; CATABOLISM; CONTROLLED STUDY; EXCITOTOXICITY; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; MICROGLIA; NEUROPROTECTION; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

AMINO ACIDS, BRANCHED-CHAIN; ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CELL MOVEMENT; CELLS, CULTURED; CYTOKINES; FREE RADICALS; GENE EXPRESSION; IMMUNOSUPPRESSIVE AGENTS; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROGLIA; PHAGOCYTOSIS; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIROLIMUS;

EID: 84874407419     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.02.001     Document Type: Article

References (47)

1. Hagenfeldt L., Eriksson S., Wahren J. Influence of leucine on arterial concentrations and regional exchange of amino acids in healthy subjects. Clin. Sci. (Lond.) 1980, 59:173-181.
2. Fernstrom J.D. Branched-chain amino acids and brain function. J. Nutr. 2005, 135:1539S-1546S.
3. Brosnan J.T., Brosnan M.E. Branched-chain amino acids: enzyme and substrate regulation. J. Nutr. 2006, 136:207S-211S.
4. Gleeson M. Interrelationship between physical activity and branched-chain amino acids. J. Nutr. 2005, 135:1591S-1595S.
5. Cole J.T., Mitala C.M., Kundu S., Verma A., Elkind J.A., Nissim I., Cohen A.S. Dietary branched chain amino acids ameliorate injury-induced cognitive impairment. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:366-371.
6. Zinnanti W.J., Lazovic J. Interrupting the mechanisms of brain injury in a model of maple syrup urine disease encephalopathy. J. Inherit. Metab. Dis. 2012, 35:71-79.
7. Zinnanti W.J., Lazovic J., Griffin K., Skvorak K.J., Paul H.S., Homanics G.E., Bewley M.C., Cheng K.C., Lanoue K.F., Flanagan J.M. Dual mechanism of brain injury and novel treatment strategy in maple syrup urine disease. Brain 2009, 132:903-918.
8. Wajner M., Coelho D.M., Barschak A.G., Araujo P.R., Pires F., Lulhier F.L.G., Vargas C.R. Reduction of large neutral amino acid concentrations in plasma and CSF of patients with maple syrup urine disease during crises. J. Inherit. Metab. Dis. 2000, 23:505-512.
9. Contrusciere V., Paradisi S., Matteucci A., Malchiodi-Albedi F. Branched-chain amino acids induce neurotoxicity in rat cortical cultures. Neurotox. Res. 2010, 17:392-398.
10. Carunchio I., Curcio L., Pieri M., Pica F., Caioli S., Viscomi M.T., Molinari M., Canu N., Bernardi G., Zona C. Increased levels of p70S6 phosphorylation in the G93A mouse model of Amyotrophic Lateral Sclerosis and in valine-exposed cortical neurons in culture. Exp. Neurol. 2010, 226:218-230.
11. Nimmerjahn A., Kirchhoff F., Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308:1314-1318.
12. Colton C.A. Heterogeneity of microglial activation in the innate immune response in the brain. J. Neuroimmune Pharmacol. 2009, 4:399-418.
13. Calder P.C. Branched-chain amino acids and immunity. J. Nutr. 2006, 136:288S-293S.
14. Levi G., Patrizio M., Bernardo A., Petrucci T.C., Agresti C. Human immunodeficiency virus coat protein gp120 inhibits the beta-adrenergic regulation of astroglial and microglial functions. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:1541-1545.
15. De Simone R., Niturad C.E., De Nuccio C., Ajmone-Cat M.A., Visentin S., Minghetti L. TGF-β and LPS modulate ADP-induced migration of microglial cells through P2Y1 and P2Y12 receptor expression. J. Neurochem. 2010, 115:450-459.
16. Minghetti L., Polazzi E., Nicolini A., Créminon C., Levi G. Interferon-gamma and nitric oxide down-regulate lipopolysaccharide-induced prostanoid production in cultured rat microglial cells by inhibiting cyclooxygenase-2 expression. J. Neurochem. 1996, 66:1963-1970.
17. Ajmone-Cat A.M., Salvatori M.L., De Simone R., Mancini M., Biagioni S., Bernardo A., Cacci E., Minghetti L. Docosahexaenoic acid modulates inflammatory and antineurogenic functions of activated microglial cells. J. Neurosci. Res. 2012, 90:575-587.
18. De Simone R., Ambrosini E., Carnevale D., Ajmone-Cat M.A., Minghetti L. NGF promotes microglial migration through the activation of its high affinity receptor: modulation by TGF-beta. J. Neuroimmunol. 2007, 190:53-60.
19. Jouvet P., Rustin P., Taylor D.L., Pocock J.M., Felderhoff-Mueser U., Mazarakis N.D., Sarraf C., Joashi U., Kozma M., Greenwood K., Edwards A.D., Mehmet H. Branched chain amino acids induce apoptosis in neural cells without mitochondrial membrane depolarization or cytochrome c release: implications for neurological impairment associated with maple syrup urine disease. Mol. Biol. Cell 2000, 11:1919-1932.
20. Ahmed Z., Shaw G., Sharma V.P., Yang C., McGowan E., Dickson D.W. Actin-binding proteins coronin-1a and IBA-1 are effective microglial markers for immunohistochemistry. J. Histochem. Cytochem. 2007, 55:687-700.
21. Kanazawa H., Ohsawa K., Sasaki Y., Kohsaka S., Imai Y. Macrophage/microglia-specific protein Iba1 enhances membrane ruffling and Rac activation via phospholipase C-gamma-dependent pathway. J. Biol. Chem. 2002, 277:20026-20032.
22. Greco A., Minghetti L. Isoprostanes as biomarkers and mediators of oxidative injury in infant and adult central nervous system diseases. Curr. Neurovasc. Res. 2004, 1:341-354.
23. Ribeiro C.A., Sgaravatti A.M., Rosa R.B., Schuck P.F., Grando V., Schmidt A.L., Ferreira G.C., Perry M.L., Dutra-Filho C.S., Wajner M. Inhibition of brain energy metabolism by the branched-chain amino acids accumulating in maple syrup urine disease. Neurochem. Res. 2008, 33:114-124.
24. Koizumi S., Shigemoto-Mogami Y., Nasu-Tada K., Shinozaki Y., Ohsawa K., Tsuda M., Joshi B.V., Jacobson K.A., Kohsaka S., Inoue K. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 2007, 446:1091-1095.
25. Dello Russo C., Lisi L., Tringali G., Navarra P. Involvement of mTOR kinase in cytokine-dependent microglial activation and cell proliferation. Biochem. Pharmacol. 2009, 78:1242-1251.
26. de Oliveira A.C., Candelario-Jalil E., Langbein J., Wendeburg L., Bhatia H.S., Schlachetzki J.C., Biber K., Fiebich B.L. Pharmacological inhibition of Akt and downstream pathways modulates the expression of COX-2 and mPGES-1 in activated microglia. J. Neuroinflammation 2012, 9:2.
27. Weichhart T., Costantino G., Poglitsch M., Rosner M., Zeyda M., Stuhlmeier K.M., Kolbe T., Stulnig T.M., Hörl W.H., Hengstschläger M., Müller M., Säemann M.D. The TSC-mTOR signaling pathway regulates the innate inflammatory response. Immunity 2008, 29:565-577.
28. Bixel M.G., Shimomura Y., Hutson S., Hamprecht B. Distribution of key enzymes of branched-chain amino acid metabolism in glial and neuronal cells in culture. J. Histochem. Cytochem. 2001, 49:407-418.
29. Murín R., Schaer A., Kowtharapu B.S., Verleysdonk S., Hamprecht B. Expression of 3-hydroxyisobutyrate dehydrogenase in cultured neural cells. J. Neurochem. 2008, 105:1176-1186.
30. De Simone R., Ajmone-Cat M.A., Minghetti L. Atypical antiinflammatory activation of microglia induced by apoptotic neurons: possible role of phosphatidylserine-phosphatidylserine receptor interaction. Mol. Neurobiol. 2004, 29:197-212.
31. Leidi M., Gotti E., Bologna L., Miranda E., Rimoldi M., Sica A., Roncalli M., Palumbo G.A., Introna M., Golay J. M2 macrophages phagocytose rituximab-opsonized leukemic targets more efficiently than m1 cells in vitro. J. Immunol. 2009, 182:4415-4422.
32. Durafourt B.A., Moore C.S., Zammit D.A., Johnson T.A., Zaguia F., Guiot M.C., Bar-Or A., Antel J.P. Comparison of polarization properties of human adult microglia and blood-derived macrophages. Glia 2012, 60:717-727.
33. Ferger A.I., Campanelli L., Reimer V., Muth K.N., Merdian I., Ludolph A.C., Witting A. Effects of mitochondrial dysfunction on the immunological properties of microglia. J. Neuroinflammation 2010, 7:45.
34. Cai D., Deng K., Mellado W., Lee J., Ratan R.R., Filbin M.T. Arginase I and polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron 2002, 35:711-719.
35. Lee J., Ryu H., Kowall N.W. Motor neuronal protection by l-arginine prolongs survival of mutant SOD1 (G93A) ALS mice. Biochem. Biophys. Res. Commun. 2009, 384:524-529.
36. Schaeffer V., Arbabi S., Garcia I.A., Knoll M.L., Cuschieri J., Bulger E.M., Maier R.V. Role of the mTOR pathway in LPS-activated monocytes: influence of hypertonic saline. J. Surg. Res. 2011, 171:769-776.
37. Dibaj P., Steffens H., Zschüntzsch J., Nadrigny F., Schomburg E.D., Kirchhoff F., Neusch C. In vivo imaging reveals distinct inflammatory activity of CNS microglia versus PNS macrophages in a mouse model for ALS. PLoS One 2011, 6:e17910.
38. Valerio A., D'Antona G., Nisoli E. Branched-chain amino acids, mitochondrial biogenesis, and healthspan: an evolutionary perspective. Aging (Albany NY) 2011, 3:464-478.
39. Maughan R.J., Depiesse F., Geyer H. The use of dietary supplements by athletes. J. Sports Sci. 2007, 25:S103-S113.
40. Pencharz P.B., Elango R., Ball R.O. Determination of the tolerable upper intake level of leucine in adult men. J. Nutr. 2012, 142:2220S-2224S.
41. Walsh A.L., Gonzalez A.M., Ratamess N.A., Kang J., Hoffman J.R. Improved time to exhaustion following ingestion of the energy drink amino impact. J. Int. Soc. Sports Nutr. 2010, 7:14.
42. Seifert S.M., Schaechter J.L., Hershorin E.R., Lipshultz S.E. Health effects of energy drinks on children, adolescents, and young adults. Pediatrics 2011, 127:511-528.
43. Hutson S.M., Lieth E., La Noue K.F. Function of leucine in excitatory neurotransmitter metabolism in the central nervous system. J. Nutr. 2001, 131:846S-850S.
44. Belli S., Vanacore N. Proportionate mortality of Italian soccer players: is amyotrophic lateral sclerosis an occupational disease?. Eur. J. Epidemiol. 2005, 20:237-242.
45. Chiò A., Benzi G., Dossena M., Mutani R., Mora G. Severely increased risk of amyotrophic lateral sclerosis among Italian professional football players. Brain 2005, 128:472-476.
46. Piscopo P., Crestini A., Adduci A., Ferrante A., Massari M., Popoli P., Vanacore N., Confaloni A. Altered oxidative stress profile in the cortex of mice fed an enriched branched-chain amino acids diet: possible link with amyotrophic lateral sclerosis?. J. Neurosci. Res. 2011, 89:1276-1283.
47. Venerosi A., Martire A., Rungi A., Pieri M., Ferrante A., Zona C., Popoli P., Calamandrei G. Complex behavioral and synaptic effects of dietary branched chain amino acids in a mouse model of amyotrophic lateral sclerosis. Mol. Nutr. Food Res. 2011, 55:541-552.