Amino Acids as biomarkers in the SOD1G93A mouse model of ALS

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 1, 2014, Pages 79-87

  Bame, Monica ^a   Grier, Robert E ^a   Needleman, Richard ^a   Brusilow, William S A ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ALS; Biomarker; Methylation; Plasma amino acid

Indexed keywords

ASPARTIC ACID; CARBAMOYL PHOSPHATE SYNTHASE; CITRULLINE; CYSTEINE; DNA METHYLTRANSFERASE 3A; GAMMA GLUTAMYLTRANSFERASE; GLUTAMATE AMMONIA LIGASE; GLUTAMIC ACID; GLUTAMINE; HISTIDINE; LYSINE; METHIONINE; METHIONINE SULFOXIMINE; ORNITHINE; PHOSPHOETHANOLAMINE; SARCOSINE;

AMINO ACID ANALYSIS; AMINO ACID BLOOD LEVEL; AMINO ACID COMPOSITION; AMINO ACID METABOLISM; AMINO ACID SYNTHESIS; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVITY; FEMALE; GRIP STRENGTH; INHIBITION KINETICS; LIFESPAN; MALE; METHYLATION; MOUSE; MSOD1 MOUSE; MUSCLE WEAKNESS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UREA CYCLE; WILD TYPE;

ALS; BIOMARKER; METHYLATION; PLASMA AMINO ACID;

AGE FACTORS; AMINO ACIDS; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BIOLOGICAL MARKERS; DISEASE MODELS, ANIMAL; FEMALE; GLUTAMATE-AMMONIA LIGASE; HUMANS; LONGEVITY; MALE; METABOLOME; METHIONINE SULFOXIMINE; METHYLATION; MICE; MICE, TRANSGENIC; MUTATION; SEX FACTORS; SUPEROXIDE DISMUTASE;

EID: 84887718141     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.10.004     Document Type: Article

References (68)

1. Dengler R. El Escorial or Awaji criteria in ALS diagnosis, what should we take?. Rom. J. Neurol. Psychiatry 2012, 123:217-218.
2. Nirmalananthan N., Greensmith L. Amyotrophic lateral sclerosis: recent advances and future therapies. Curr. Opin. Neurol. 2005, 18:712-719.
3. Al-Chalabi A., Jones A., Troakes C., King A., Al-Sarraj S., den Berg L.H. The genetics and neuropathology of amyotrophic lateral sclerosis. Acta Neuropathol. 2012, 124:339-352.
4. Turner M.R., Kiernan M.C., Leigh P.N., Talbot K. Biomarkers in amyotrophic lateral sclerosis. Lancet Neurol. 2009, 8:94-109.
5. Pradat P.-F., Dib M. Biomarkers in amyotrophic lateral sclerosis: facts and future horizons. Mol. Diagn. Ther. 2009, 13:115-125.
6. Nakano Y., Hirayama K., Terao K. Hepatic ultrastructural changes and liver dysfunction in amyotrophic lateral sclerosis. Arch. Neurol. 1987, 44:103-106.
7. Abmayr S., Weydt P. Skeletal muscle in amyotrophic lateral sclerosis: emerging concepts and therapeutic implications. Phys. Med. Rehabil. Clin. N. Am. 2005, 16:1091-1097. (xi-xii).
8. Iłzecka J., Stelmasiak Z., Solski J., Wawrzycki S., Szpetnar M. Plasma amino acids percentages in amyotrophic lateral sclerosis patients 2003, 25:69-73.
9. Perry T.L., Krieger C., Hansen S., Eisen A. Amyotrophic lateral sclerosis: amino acid levels in plasma and cerebrospinal fluid. Ann. Neurol. 1990, 28:12-17.
10. Camu W., Billiard M., Baldy-Moulinier M. Fasting plasma and CSF amino acid levels in amyotrophic lateral sclerosis: a subtype analysis. Acta Neurol. Scand. 1993, 88:51-55.
11. Ghoddoussi F., Galloway M.P., Jambekar A., Bame M., Needleman R., Brusilow W.S.A. Methionine sulfoximine, an inhibitor of glutamine synthetase, lowers brain glutamine and glutamate in a mouse model of ALS. J. Neurosci. 2010, 290:41-47.
12. Brusilow S.W. Phenylacetylglutamine may replace urea as a vehicle for waste nitrogen excretion 1991, 29:147-150.
13. Meister A. Glutamine synthetase from mammalian tissues. Methods Enzymol. 1985, 113:185-199.
14. Pierson D. A rapid colorimetric assay for carbamyl synthetase I. J. Biochem. Biophys. Methods 1980, 3:31-37.
15. Ronzio R.A., Meister A. Phosphorylation of methionine sulfoximine by glutamine synthetase. Proc. Natl. Acad. Sci. U. S. A. 1968, 59:164-170.
16. Bame M., Pentiak P., Needleman R., Brusiow W. Effect of sex on lifespan, disease progression, and the response to methionine sulfoximine in the SOD1 G93A mouse model for ALS. Gend. Med. 2012, 9:524-535.
17. Cohen J. A power primer. Psychol. Bull. 1992, 112:155-159.
18. McCombe P., Henderson R. Effects of gender in amyotrophic lateral sclerosis. Gend. Med. 2010, 7:557-570.
19. Frutiger K., Lukas T.J., Gorrie G., Ajroud-Driss S., Siddique T. Gender difference in levels of Cu/Zn superoxide dismutase (SOD1) in cerebrospinal fluid of patients with amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2008, 9:184-187.
20. Hadano S., Otomo A., Kunita R., Suzuki-Utsunomiya K., Akatsuka A., Koike M., Aoki M., Uchiyama Y., Itoyama Y., Ikeda J.-E. Loss of ALS2/Alsin exacerbates motor dysfunction in a SOD1-expressing mouse ALS model by disturbing endolysosomal trafficking. PLoS One 2010, 5:e9805.
21. Bame M. Understanding the gender-based mechanism of MSO in ALS mice: a metabolic characterization of the SOD1G93A mouse model 2012, (Ph.D. Thesis), Wayne State University School of Medicine.
22. Blasco H., Guennoc A.-M., Veyrat-Durebex C., Gordon P.H., Andres C.R., Camu W., Corcia P. Amyotrophic lateral sclerosis: a hormonal condition?. Amyotroph. Lateral Scler. 2012, 13:585-588.
23. Blin M., Crusio W.E., Hévor T., Cloix J.-F. Chronic inhibition of glutamine synthetase is not associated with impairment of learning and memory in mice. Brain Res. Bull. 2002, 57:11-15.
24. Lawton K.A., Cudkowicz M.E., Brown M.V., Alexander D., Caffrey R., Wulff J.E., Bowser R., Lawson R., Jaffa M., Milburn M.V., Ryals J.A., Berry J.D. Biochemical alterations associated with ALS. Amyotroph. Lateral Scler. 2012, 13:110-118.
25. Iwasaki Y., Ikeda K., Kinoshita M. Plasma amino acid levels in patients with amyotrophic lateral sclerosis. J. Neurosci. 1992, 107:219-222.
26. Lawton K.A., Berger A., Mitchell M., Milgram K.E., Evans A.M., Guo L., Hanson R.W., Kalhan S.C., Ryals J.A., Milburn M.V. Analysis of the adult human plasma metabolome. Pharmacogenomics 2008, 9:383-397.
27. Serio A., Bilican B., Barmada S.J. Astrocyte pathology and the absence of non-cell autonomy in an induced pluripotent stem cell model of TDP-43 proteinopathy. Proc. Natl. Acad. Sci. 2013, 110:4697-4702.
28. Phatnani H.P., Guarnieri P., Friedman B.A., Carrasco M.A., Muratet M., O'Keeffe S., Nwakeze C., Pauli-Behn F., Newberry K.M., Meadows S.K., Tapia J.C., Myers R.M., Maniatis T. Intricate interplay between astrocytes and motor neurons in ALS. Proc. Natl. Acad. Sci. 2013, 110:E756-E765.
29. Wuolikainen A., Andersen P.M., Moritz T., Marklund S.L., Antti H. ALS patients with mutations in the SOD1 gene have an unique metabolomic profile in the cerebrospinal fluid compared with ALS patients without mutations. Mol. Genet. Metab. 2012, 105:472-478.
30. Chiu A.Y., Zhai P., Dal Canto M.C., Peters T.M., Kwon Y.W., Prattis S.M., Gurney M.E. Age-dependent penetrance of disease in a transgenic mouse model of familial amyotrophic lateral sclerosis. Mol. Cell 1995, 6:349-362.
31. Dupuis L., Dupuis L., Oudart H., Oudart H., René F., René F., Gonzalez de Aguilar J.-L., Gonzalez de Aguilar J.-L., Loeffler J.-P., Loeffler J.-P. Evidence for defective energy homeostasis in amyotrophic lateral sclerosis: benefit of a high-energy diet in a transgenic mouse model. Proc. Natl. Acad. Sci. 2004, 101:11159-11164.
32. Dobrowolny G., Aucello M., Rizzuto E., Beccafico S., Mammucari C., Bonconpagni S., Belia S., Wannenes F., Nicoletti C., Del Prete Z., Rosenthal N., Molinaro M., Protasi F., Fanò G., Sandri M., Musarò A. Skeletal muscle is a primary target of SOD1G93A-mediated toxicity. Cell Metab. 2008, 8:425-436.
33. Finkelstein A., Kunis G., Seksenyan A., Ronen A., Berkutzki T., Azoulay D., Koronyo-Hamaoui M., Schwartz M. Abnormal changes in NKT cells, the IGF-1 axis, and liver pathology in an animal model of ALS. PLoS One 2011, 6:e22374.
34. Dodge J.C., Treleaven C.M., Fidler J.A., Tamsett T.J., Bao C., Searles M., Taksir T.V., Misra K., Sidman R.L., Cheng S.H., Shihabuddin L.S. Metabolic signatures of amyotrophic lateral sclerosis reveal insights into disease pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 2013, 108:10812-10817.
35. Fuso A. The 'golden age' of DNA methylation in neurodegenerative diseases. Neurobiol. Aging 2012, 1-12.
36. Xu Z., Li X. DNA methylation in neurodegenerative disorders. Curr. Transl. Geriatr. Gerontol. Rep. 2012, 1:199-205.
37. Xu Z., Li H., Jin P. Epigenetics-based therapeutics for neurodegenerative disorders. Curr. Transl. Geriatr. Gerontol. Rep. 2012, 1:229-236.
38. Morahan J.M., Yu B., Trent R.J., Pamphlett R. A genome-wide analysis of brain DNA methylation identifies new candidate genes for sporadic amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2009, 10:418-429.
39. Zhu J.W., Yuan J.F., Yang H.M., Wang S.T., Zhang C.G., Sun L.L., Yang H., Zhang H. Extracellular cysteine (Cys)/cystine (CySS) redox regulates metabotropic glutamate receptor 5 activity. Biochimie 2012, 94:617-627.
40. Levring T.B., Hansen A.K., Nielsen B.L., Kongsbak M., von Essen M.R., Woetmann A., Odum N., Bonefeld C.M., Geisler C. Activated human CD4 T cells express transporters for both cysteine and cystine. Sci. Rep. 2012, 2:266.
41. Bridges R., Lutgen V., Lobner D., Baker D.A. Thinking outside the cleft to understand synaptic activity: contribution of the cystine-glutamate antiporter (System xc-) to normal and pathological glutamatergic signaling. Pharmacol. Rev. 2012, 64:780-802.
42. Dröge W., Gross A., Hack V., Kinscherf R., Schykowski M., Bockstette M., Mihm S., Galter D. Role of cysteine and glutathione in HIV infection and cancer cachexia: therapeutic intervention with N-acetylcysteine. Adv. Pharmacol. 1997, 38:581-600.
43. Hack V., Schmid D., Breitkreutz R., Stahl-Henning C., Drings P., Kinscherf R., Taut F., Holm E., Dröge W. Cystine levels, cystine flux, and protein catabolism in cancer cachexia, HIV/SIV infection, and senescence. FASEB J. 1997, 11:84-92.
44. Vargas M.R., Johnson D.A., Johnson J.A. Decreased glutathione accelerates neurological deficit and mitochondrial pathology in familial ALS-linked hSOD1G93A mice model. Neurobiol. Dis. 2011, 43:543-551.
45. D'Alessandro G., Calcagno E., Tartari S., Rizzardini M., Invernizzi R.W., Cantoni L. Glutamate and glutathione interplay in a motor neuronal model of amyotrophic lateral sclerosis reveals altered energy metabolism. Neurobiol. Dis. 2011, 43:346-355.
46. Chestnut B.A., Chang Q., Price A., Lesuisse C., Wong M., Martin L.J. Epigenetic regulation of motor neuron cell death through DNA methylation. J. Neurosci. 2011, 31:16619-16636.
47. Robertson K.D. DNA methylation and human disease. Nat. Rev. Genet. 2005, 6:597-610.
48. Zoccolella S., Simone I.L., Lamberti P., Samarelli V., Tortelli R., Serlenga L., Logroscino G. Elevated plasma homocysteine levels in patients with amyotrophic lateral sclerosis 2008, 70:222-225.
49. Mudd S., Bronson J., Bronson M., Jacobs R., Stabler S., Allen R., Vance D., Wagner C. Methyl balance and transmethylation fluxes in humans. Am. J. Clin. Nutr. 2007, 85:19-25.
50. Socała K., Nieoczym D., Rundfeldt C., Wlaź P. Effects of sarcosine, a glycine transporter type 1 inhibitor, in two mouse seizure models. Pharmacol. Rep. 2010, 62:392-397.
51. Dever J.T., Elfarra A.A. The biochemical and toxicological significance of hypermethionemia: new insights and clinical relevance. Expert Opin. Drug Metab. Toxicol. 2010, 6:1333-1346.
52. Mato J.M., Martínez-Chantar M.L., Lu S.C. Methionine metabolism and liver disease. Nutrition 2008, 28:273-293.
53. Patten B.M., Harati Y., Acosta L., Jung S.S., Felmus M.T. Free amino acid levels in amyotrophic lateral sclerosis. Ann. Neurol. 1978, 3:305-309.
54. Stuerenburg H.J., Petersen K., Buhmann C., Rosenkranz M., Baeumer T., Thomasius R. Plasma amino acids in ecstasy users 2003, 24:348-349.
55. Klunk W.E., McClure R.J., Pettegrew J.W. Possible roles of l-phosphoserine in the pathogenesis of Alzheimer's disease. Mol. Chem. Neuropathol. 1991, 15:51-73.
56. Sasabe J., Aiso S. Aberrant control of motoneuronal excitability in amyotrophic lateral sclerosis: excitatory glutamate/D-serine vs. inhibitory glycine/gamma-aminobutanoic acid (GABA). Chem. Biodivers. 2010, 7:1479-1490.
57. Sasabe J., Chiba T., Yamada M., Okamoto K., Nishimoto I., Matsuoka M., Aiso S. D-Serine is a key determinant of glutamate toxicity in amyotrophic lateral sclerosis. EMBO J. 2007, 26:4149-4159.
58. Lobsiger C.S., Boillée S., Cleveland D.W. Toxicity from different SOD1 mutants dysregulates the complement system and the neuronal regenerative response in ALS motor neurons. Proc. Natl. Acad. Sci. 2007, 104:7319-7326.
59. Ellison D.W., Beal M.F., Martin J.B. Phosphoethanolamine and ethanolamine are decreased in Alzheimer's disease and Huntington's disease. Brain Res. 1987, 417:389-392.
60. Nikkilä J., Sysi-Aho M., Ermolov A., Seppänen-Laakso T., Simell O., Kaski S., Oresic M. Gender-dependent progression of systemic metabolic states in early childhood. Mol. Syst. Biol. 2008, 4:197.
61. Mittelstrass K., Ried J.S., Yu Z., Krumsiek J., Gieger C., Prehn C., Roemisch-Margl W., Polonikov A., Peters A., Theis F.J. Discovery of sexual dimorphisms in metabolic and genetic biomarkers. PLoS Genet. 2011, 7:e1002215.
62. Sreekumar A., Poisson L.M., Rajendiran T.M., Khan A.P., Cao Q., Yu J., Laxman B., Mehra R., Lonigro R.J., Li Y., Nyati M.K., Ahsan A., Kalyana-Sundaram S., Han B., Cao X., Byun J., Omenn G.S., Ghosh D., Pennathur S., Alexander D.C., Berger A., Shuster J.R., Wei J.T., Varambally S., Beecher C., Chinnaiyan A.M. Metabolomic profiles delineate potential role for sarcosine in prostate cancer progression. Nature 2009, 457:910-914.
63. Folbergrová J., Passonneau J.V., Lowry O.H., Schulz D.W. Glycogen, ammonia and related metabolities in the brain during seizures evoked by methionine sulphoximine. J. Neurochem. 1969, 16:191-203.
64. Yudkoff M., Daikhin Y., Nissim I., Nissim I. Acidosis and astrocyte amino acid metabolism. Neurochem. Int. 2000, 36:329-339.
65. Šafránek R., Holeček M., Kadlčíková J., Šprongl L., Mišlanová C., Kukan M., Chládek J. Effect of acute acidosis on protein and amino acid metabolism in rats. Clin. Nutr. 2003, 22:437-443.
66. Sellinger O.Z., Schatz R.A., Gregor P. Cerebral methylations in epileptogenesis. Adv. Neurol. 1986, 44:465-473.
67. Schatz R.A., Sellinger O.Z. Effect of methionine and methionine sulphoximine on rat brain S-adenosyl methionine levels. J. Neurochem. 1975, 24:63-66.
68. Schatz R.A., Sellinger O.Z. The elevation of cerebral histamine-N-and catechol-O-methyl transferase activities by L-methionine-dl-sulfoximine. J. Neurochem. 1975, 25:73-78.