The heme degradation pathway is a promising serum biomarker source for the early detection of Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 19, Issue 3, 2010, Pages 1081-1091

  Mueller, Claudius ^a,b   Zhou, Weidong ^b   Vanmeter, Amy ^b   Heiby, Michael ^b   Magaki, Shino ^a   Ross, Mark M ^b   Espina, Virginia ^b   Schrag, Matthew ^a   Dickson, Cindy ^a   Liotta, Lance A ^b   Kirsch, Wolff M ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GEORGE MASON UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Biomarker; BLVR; BVR; Complement factor H; Heme; Heme oxyengase 1; Phospholipase D1; Prosaposin; S100A7; Serum

Indexed keywords

BILIVERDIN; BILIVERDIN OXIREDUCTASE B; BILIVERDIN REDUCTASE; BIOLOGICAL MARKER; HEME; MATRIX METALLOPEPTIDASE 9; OXIDOREDUCTASE; OXYGENASE; OXYGENASE 1; PHOSPHOLIPASE D1; PROSAPOSIN; PSORIASIN; UNCLASSIFIED DRUG;

AGED; ALZHEIMER DISEASE; ARTICLE; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; DISEASE COURSE; FEMALE; HUMAN; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; MILD COGNITIVE IMPAIRMENT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MICROARRAY; PROTEIN SYNTHESIS; TANDEM MASS SPECTROMETRY;

EID: 77149123638     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-1303     Document Type: Article

References (48)

1. Petersen RC (2004) Mild cognitive impairment as a diagnostic entity. J Intern Med 256, 183-194.
2. Schott JM, Kennedy J, Fox NC (2006) New developments in mild cognitive impairment and Alzheimer's disease. Curr Opin Neurol 19, 552-558.
3. Clark CM, Xie S, Chittams J, Ewbank D, Peskind E, Galasko D, Morris JC, McKeel DW, Farlow M, Weitlauf SL, Quinn J, Kaye J, Knopman D, Arai H, Doody RS, DeCarli C, Leight S, Lee VM, Trojanowski JQ (2003) Cerebrospinal fluid tau and beta-amyloid: how well do these biomarkers reflect autopsyconfirmed dementia diagnoses? Arch Neurol 60, 1696-1702.
4. Andreasen N, Sjögren M, Blennow K (2003) CSF markers for Alzheimer's disease: total tau, phospho-tau and Abeta42. World J Biol Psychiatry 4, 147-155.
5. Nagy Z (2007) The dysregulation of the cell cycle and the diagnosis of Alzheimer's disease. Biochim Biophys Acta 1772, 402-408.
6. Palotas A, Kalman J, Palotas M, Juhasz A, Janka Z, Penke B (2002) Beta-amyloid-induced increase in the resting intracellular calcium concentration gives support to tell Alzheimer lymphocytes from control ones. Brain Res Bull 58, 203-205.
7. Kalman J, Kitajka K, Pakaski M, Zvara A, Juhasz A,Vincze G, Janka Z, Puskas LG (2005) Gene expression profile analysis of lymphocytes from Alzheimer's patients. Psychiatr Genet. 15, 1-6.
8. Squitti R, Pasqualetti P, Dal Forno G, Moffa F, Cassetta E, Lupoi D, Vernieri F, Rossi L, Baldassini M, Rossini PM (2005) Excess of serum copper not related to ceruloplasmin in Alzheimer disease. Neurology 64, 1040-1046.
9. Kozubski W, Swiderek M, Kloszewska I, Gwozdzinski K, Watala C (2002) Blood platelet membrane fluidity and the exposition of membrane protein receptors in Alzheimer disease (AD) patientsflpreliminary Study. Alzheimer Dis Assoc Disord 16, 52-54.
10. Ray S, Britschgi M, Herbert C, Takeda-Uchimura Y, Boxer A, Blennow K, Friedman LF, Galasko DR, Jutel M, Karydas A, Kaye JA, Leszek J, Miller BL, Minthon L, Quinn JF, Rabinovici GD, Robinson WH, Sabbagh MN, So YT, Sparks DL, Tabaton M, Tinklenberg J, Yesavage JA, Tibshirani R,Wyss-Coray T (2007) Classification and prediction of clinical Alzheimer's diagnosis based on plasma signaling proteins. Nat Med 13, 1359-1362.
11. Song F, Poljak A, Smythe GA, Sachdev P (2009) Plasma biomarkers for mild cognitive impairment and Alzheimer's disease. Brain Res Rev 61, 69-80.
12. Liotta LA, Ferrari M, Petricoin E (2003) Clinical proteomics: written in blood. Nature 425, 905.
13. Hye A, Lynham S, Thambisetty M, Causevic M, Campbell J, Byers HL, Hooper C, Rfisdfik F, Tabrizi SJ, Banner S, Shaw CE, Foy C, Poppe M, Archer N, Hamilton G, Powell J, Brown RG, Sham P, Ward M, Lovestone S (2006) Proteome-based plasma biomarkers for Alzheimer's disease. Brain 129, 3042-3050.
14. Lowenthal MS, Mehta AI, Frogale K, Bandle RW, Araujo RP, Hood BL, Veenstra TD, Conrads TP, Goldsmith P, Fishman D, Petricoin EF, Liotta LA(2005) Analysis of albumin-associated peptides and proteins from ovarian cancer patients. Clin Chem 51, 1933-1945.
15. Lopez MF, Mikulskis A, Kuzdzal S, Bennett DA, Kelly J, Golenko E, DiCesare J, Denoyer E, Patton WF, Ediger R, Sapp L, Ziegert T, Lynch C, Kramer S, Whiteley GR, Wall MR, Mannion DP, Cioppa GD, Rakitan JS,Wolfe GM (2005) High-resolution serum proteomic profiling of Alzheimer disease samples reveals disease-specific, carrier-protein-bound mass signatures. Clin Chem 51, 1946-1954.
16. Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E (1999) Mild cognitive impairment: clinical characterization and outcome. Arch. Neurol 56, 303-308. (Pubitemid 29120227)
17. Reisberg B (2007) Global measures: utility in defining and measuring treatment response in dementia. Int Psychogeriatr 19, 421-456.
18. Kirsch W, McAuley G, Holshouser B, Petersen F, Ayaz M, Vinters HV, Dickson C, Haacke EM, Britt III W, Larsen J, Kim I, Mueller C, Schrag M, Kido D (2009) Serial Susceptibility Weighted MRI Measures Brain Iron and Microbleeds in Dementia. J Alzheimers Dis 17, 599-609.
19. Elias JE, Gygi SP (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Meth 4, 207-214.
20. Paweletz CP, Charboneau L, Bichsel VE, Simone NL, Chen T, Gillespie JW, Emmert-Buck MR, Roth MJ, Petricoin III EF, Liotta LA (2001) Reverse phase protein microarrays which capture disease progression show activation of pro-survival pathways at the cancer invasion front. Oncogene 20, 1981-1989.
21. VanMeter A, Signore M, Pierobon M, Espina V, Liotta LA, Petricoin EF (2007) Reverse-phase protein microarrays: application to biomarker discovery and translational medicine. Expert Rev Mol Diagn 7, 625-633.
22. Pereira PJ, Macedo-Ribeiro S, Ṕarraga A, Ṕerez-Luque R, Cunningham O, Darcy K, Mantle TJ, Coll M (2001) Structure of human biliverdin IXbeta reductase, an early fetal bilirubin IXbeta producing enzyme. Nat Struct Biol 8, 215-220
23. Shalloe F, Elliott G, Ennis O, Mantle TJ (1996) Evidence that biliverdin-IX beta reductase and flavin reductase are identical. Biochem J 316 (Pt 2), 385-387.
24. Vaccaro AM, Salvioli R, Tatti M, Ciaffoni F (1999) Saposins and their interaction with lipids. Neurochem Res 24, 307-314.
25. Grimm MOW, Grimm HS, Pätzold AJ, Zinser EG, Halonen R, Duering M, Tschäpe JA, De Strooper B, Müller U, Shen J, Hartmann T (2005) Regulation of cholesterol and sphingomyelin metabolism by amyloid-beta and presenilin. Nat. Cell Biol 7, 1118-1123.
26. Newman M, Tucker B, Nornes S, Ward A, Lardelli M (2009) Altering presenilin gene activity in zebrafish embryos causes changes in expression of genes with potential involvement in Alzheimer's disease pathogenesis. J Alzheimers Dis 16, 133-147.
27. Cai D, Netzer WJ, Zhong M, Lin Y, Du G, Frohman M, Foster DA, Sisodia SS, Xu H, Gorelick FS, Greengard P (2006) Presenilin-1 uses phospholipase D1 as a negative regulator of beta-amyloid formation. Proc Natl Acad Sci U S A 103, 1941-1946.
28. Jin J, Kim N, Lee Y, Kim Y, Choi E, Kozlowski PB, Park MH, Kim H, Min DS (2006) Phospholipase D1 is up-regulated in the mitochondrial fraction from the brains of Alzheimer's disease patients. Neurosci Lett 407, 263-267.
29. Zipfel PF, Skerka C (1999) FHL-1/reconectin: a human complement and immune regulator with cell-adhesive function. Immunol Today 20, 135-140.
30. Strohmeyer R, Shen Y, Rogers J (2000) Detection of complement alternative pathway mRNA and proteins in the Alzheimer's disease brain. Brain Res Mol Brain Res 81, 7-18.
31. Qin W, Ho L, Wang J, Peskind E, Pasinetti GM (2009) S100A7, a novel Alzheimer's disease biomarker with nonamyloidogenic alpha-secretase activity acts via selective promotion of ADAM-10. PLoS ONE 4, e4183.
32. SmithMA,Kutty RK, Richey PL,Yan SD, Stern D,Chader GJ, Wiggert B, Petersen RB, Perry G (1994) Heme oxygenase-1 is associated with the neurofibrillary pathology of Alzheimer's disease. Am J Pathol 145, 42-47.
33. Schipper HM, Bennett DA, Liberman A, Bienias JL, Schneider JA, Kelly J, Arvanitakis Z (2006) Glial heme oxygenase-1 expression in Alzheimer disease and mild cognitive impairment. Neurobiol Aging 27, 252-261.
34. Dwyer BE, Smith MA, Richardson SL, Perry G, Zhu X (2009) Down-regulation of aminolevulinate synthase, the ratelimiting enzyme for heme biosynthesis in Alzheimer's disease. Neurosci Lett 460, 180-184.
35. Atamna H, Frey WH (2004) A role for heme in Alzheimer's disease: Heme binds amyloid beta and has altered metabolism. Proc Natl Acad Sci U S A 101, 11153-11158.
36. Atamna H, Boyle K (2006) Amyloid-beta peptide binds with heme to form a peroxidase: relationship to the cytopathologies of Alzheimer's disease. Proc Natl Acad Sci U S A 103, 3381-3386.
37. Atamna H, Frey WH (2007) Mechanisms of mitochondrial dysfunction and energy deficiency in Alzheimer's disease. Mitochondrion 7, 297-310.
38. Kimpara T, Takeda A, Yamaguchi T, Arai H, Okita N, Takase S, Sasaki H, Itoyama Y (2000) Increased bilirubins and their derivatives in cerebrospinal fluid in Alzheimer's disease. Neurobiol Aging 21, 551-554.
39. Kim T, Pae C, Yoon S, Jang W, Lee NJ, Kim J, Lee S, Lee C, Paik I, Lee C (2006) Decreased plasma antioxidants in patients with Alzheimer's disease. Int J Geriatr Psychiatry 21, 344-348.
40. Schipper HM, Chertkow H, Mehindate K, Frankel D, Melmed C, Bergman H (2000) Evaluation of heme oxygenase-1 as a systemic biological marker of sporadic AD. Neurology 54, 1297-1304.
41. Maes OC, Kravitz S, Mawal Y, Su H, Liberman A, Mehindate K, Berlin D, Sahlas DJ, Chertkow HM, Bergman H, Melmed C, Schipper HM(2006) Characterization of alpha1-antitrypsin as a heme oxygenase-1 suppressor in Alzheimer plasma. Neurobiol Dis 24, 89-100.
42. Maines MD (2005) New insights into biliverdin reductase functions: linking heme metabolism to cell signaling. Physiology (Bethesda) 20, 382-389.
43. Lerner-Marmarosh N, Miralem T, Gibbs PEM, Maines MD (2008) Human biliverdin reductase is an ERK activator; hBVR is an ERK nuclear transporter and is required for MAPK signaling. Proc Natl Acad Sci U S A 105, 6870-6875.
44. Longo VD, Finch CE (2003) Evolutionary medicine: from dwarf model systems to healthy centenarians? Science 299, 1342-1346.
45. Puglielli L (2008) Aging of the brain, neurotrophin signaling, and Alzheimer's disease: is IGF1-R the common culprit? Neurobiol Aging 29, 795-811.
46. Steen E, Terry BM, Rivera EJ, Cannon JL, Neely TR, Tavares R, Xu XJ, Wands JR, de la Monte SM (2005) Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease-is this type 3 diabetes? J Alzheimers Dis 7, 63-80.
47. Hasan W, Smith HJ, Ting AY, Smith PG (2005) Estrogen alters trkA and p75 neurotrophin receptor expression within sympathetic neurons. J Neurobiol 65, 192-204.
48. Tang MX, Jacobs D, Stern Y, Marder K, Schofield P, Gurland B, Andrews H, Mayeux R (1996) Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease. Lancet 348, 429-432.