| Journal of Molecular Psychiatry | |
| Mass spectrometry as a tool for studying autism spectrum disorder | |
| Costel C Darie4  Johannes Thome1  Tanja Maria Michel3  Jeanne P Ryan2  Stefanie Russell2  Izabela Sokolowska4  Armand G Ngounou Wetie4  Alisa G Woods4  | |
| [1] College of Medicine, Swansea University, Singleton Park, Swansea, SA2 8PP, UK;Department of Psychology, State University of New York at Plattsburgh, 101 Broad Street, Plattsburgh, NY 12901, USA;Department of Psychiatry, University of Rostock, Gehlsheimer Straße 20, D-18147, Rostock, Germany;Biochemistry and Proteomics Group Department of Chemistry and Biomolecular Science, Clarkson University, 8 Clarkson Avenue, Potsdam, NY 13699-5810, USA | |
| 关键词: Autism spectrum disorder; Protein biomarkers; Proteomics; Mass spectrometry; | |
| Others : 820477 DOI : 10.1186/2049-9256-1-6 |
|
| received in 2012-10-02, accepted in 2012-11-13, 发布年份 2013 | |
PDF
|
|
【 摘 要 】
Autism spectrum disorders (ASDs) are increasing in incidence but have an incompletely understood etiology. Tools for uncovering clues to the cause of ASDs and means for diagnoses are valuable to the field. Mass Spectrometry (MS) has been a useful method for evaluating differences between individuals with ASDs versus matched controls. Different biological substances can be evaluated using MS, including urine, blood, saliva, and hair. This technique has been used to evaluate relatively unsupported hypotheses based on introduction of exogenous factors, such as opiate and heavy metal excretion theories of ASDs. MS has also been used to support disturbances in serotonin-related molecules, which have been more consistently observed in ASDs. Serotonergic system markers, markers for oxidative stress, cholesterol system disturbances, peptide hypo-phosphorylation and methylation have been measured using MS in ASDs, although further analyses with larger numbers of subjects are needed (as well as consideration of behavioral data). Refinements in MS and data analysis are ongoing, allowing for the possibility that future studies examining body fluids and specimens from ASD subjects could continue to yield novel insights. This review summarizes MS investigations that have been conducted to study ASD to date and provides insight into future promising applications for this technique, with focus on proteomic studies.
【 授权许可】
2013 Woods et al.; licensee BioMed Central Ltd.
【 预 览 】
| Files | Size | Format | View |
|---|---|---|---|
| 20140712043734778.pdf | 724KB | ||
| Figure 3. | 61KB | Image | |
| Figure 2. | 53KB | Image | |
| Figure 1. | 42KB | Image |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
【 参考文献 】
- [1]DiCicco-Bloom E, Lord C, Zwaigenbaum L, Courchesne E, Dager SR, Schmitz C, Schultz RT, Crawley J, Young LJ: The developmental neurobiology of autism spectrum disorder. J Neurosci 2006, 26(26):6897-6906.
- [2]APA: Diagnostic and Statistical Manual of Mental Disorders. American Psychiatric Association: Fourth Edition, Text Revision. Arlington, VA; 2000.
- [3]Autism, Developmental Disabilities Monitoring Network Surveillance Year Principal I, Centers for Disease C, Prevention: Prevalence of autism spectrum disorders--Autism and Developmental Disabilities Monitoring Network, 14 sites, United States, 2008. Morb Mortal Wkly Rep Surveill Summ 2012, 61(3):1-19.
- [4]Dettmer K, Hanna D, Whetstone P, Hansen R, Hammock BD: Autism and urinary exogenous neuropeptides: development of an on-line SPE-HPLC-tandem mass spectrometry method to test the opioid excess theory. Anal Bioanal Chem 2007, 388(8):1643-1651.
- [5]Tanguay PE: Autism in DSM-5. Am J Psychiatry 2011, 168(11):1142-1144.
- [6]Matson JL, Kozlowski AM, Hattier MA, Horovitz M, Sipes M: DSM-IV vs DSM-5 diagnostic criteria for toddlers with Autism. Dev Neurorehabil 2012, 15(3):185-190.
- [7]Zappella M: Reversible autism and intellectual disability in children. Am J Med Genet C Semin Med Genet 2012, 160C(2):111-117.
- [8]Lovaas OI: Behavioral treatment and normal educational and intellectual functioning in young autistic children. J Consult Clin Psychol 1987, 55(1):3-9.
- [9]McEachin JJ, Smith T, Lovaas OI: Long-term outcome for children with autism who received early intensive behavioral treatment. AJMR 1993, 97(4):359-372. discussion 373–391
- [10]Sallows GO, Graupner TD: Intensive behavioral treatment for children with autism: four-year outcome and predictors. AJMR 2005, 110(6):417-438.
- [11]Leskovec TJ, Rowles BM, Findling RL: Pharmacological treatment options for autism spectrum disorders in children and adolescents. Harv Rev Psychiatry 2008, 16(2):97-112.
- [12]Myers SM: The status of pharmacotherapy for autism spectrum disorders. Expert Opin Pharmacother 2007, 8(11):1579-1603.
- [13]Rogers SJ, Vismara LA: Evidence-based comprehensive treatments for early autism. J Clin Child Adolesc Psychol 2008, 37(1):8-38.
- [14]Hagerman R, Lauterborn J, Au J, Berry-Kravis E: Fragile X syndrome and targeted treatment trials. Results Probl Cell Differ 2012, 54:297-335.
- [15]Michel TM, Sheldrick AJ, Frentzel TG, Herpertz-Dahlmann B, Herpertz S, Habel U, Bruegmann E, Schneider K: Schneider F: [Evaluation of diagnostic and therapeutic services in German university hospitals for adults with autism spectrum disorder (ASD)]. Fortschr Neurol Psychiatr 2010, 78(7):402-413.
- [16]Simonoff E, Jones CR, Pickles A, Happe F, Baird G, Charman T: Severe mood problems in adolescents with autism spectrum disorder. J Child Psychol Psychiatry 2012.
- [17]Frustaci A, Neri M, Cesario A, Adams JB, Domenici E, Dalla Bernardina B, Bonassi S: Oxidative stress-related biomarkers in autism: Systematic review and meta-analyses. Free Radic Biol Med 2012, 52(10):2128-2141.
- [18]Conciatori M, Stodgell CJ, Hyman SL, O'Bara M, Militerni R, Bravaccio C, Trillo S, Montecchi F, Schneider C, Melmed R: Association between the HOXA1 A218G polymorphism and increased head circumference in patients with autism. Biol Psychiatry 2004, 55(4):413-419.
- [19]Freitag CM, Staal W, Klauck SM, Duketis E, Waltes R: Genetics of autistic disorders: review and clinical implications. Eur Child Adolesc Psychiatry 2010, 19(3):169-178.
- [20]Hu VW, Nguyen A, Kim KS, Steinberg ME, Sarachana T, Scully MA, Soldin SJ, Luu T, Lee NH: Gene expression profiling of lymphoblasts from autistic and nonaffected sib pairs: altered pathways in neuronal development and steroid biosynthesis. PLoS One 2009, 4(6):e5775.
- [21]State MW, Levitt P: The conundrums of understanding genetic risks for autism spectrum disorders. Nat Neurosci 2011, 14(12):1499-1506.
- [22]Bailey A, Le Couteur A, Gottesman I, Bolton P, Simonoff E, Yuzda E, Rutter M: Autism as a strongly genetic disorder: evidence from a British twin study. Psychol Med 1995, 25(1):63-77.
- [23]Le Couteur A, Bailey A, Goode S, Pickles A, Robertson S, Gottesman I, Rutter M: A broader phenotype of autism: the clinical spectrum in twins. J Child Psychol Psychiatry 1996, 37(7):785-801.
- [24]Betancur C: Etiological heterogeneity in autism spectrum disorders: more than 100 genetic and genomic disorders and still counting. Brain Res 2011, 1380:42-77.
- [25]Nickl-Jockschat T, Michel TM: Genetic and brain structure anomalies in autism spectrum disorders. Towards an understanding of the aetiopathogenesis? Nervenarzt 2011, 82(5):618-627.
- [26]Neale BM, Kou Y, Liu L, Ma'ayan A, Samocha KE, Sabo A, Lin CF, Stevens C, Wang LS, Makarov V: Patterns and rates of exonic de novo mutations in autism spectrum disorders. Nature 2012, 485(7397):242-245.
- [27]Leblond CS, Heinrich J, Delorme R, Proepper C, Betancur C, Huguet G, Konyukh M, Chaste P, Ey E, Rastam M: Genetic and functional analyses of SHANK2 mutations suggest a multiple hit model of autism spectrum disorders. PLoS Genet 2012, 8(2):e1002521.
- [28]Gurrieri F: Working up autism: The practical role of medical genetics. Am J Med Genet C Semin Med Genet 2012, 160C(2):104-110.
- [29]Lee TL, Raygada MJ, Rennert OM: Integrative gene network analysis provides novel regulatory relationships, genetic contributions and susceptible targets in autism spectrum disorders. Gene 2012, 496(2):88-96.
- [30]Nickl-Jockschat T, Michel TM: The role of neurotrophic factors in autism. Mol Psychiatry 2011, 16(5):478-490.
- [31]Theoharides TC, Kempuraj D, Redwood L: Autism: an emerging 'neuroimmune disorder' in search of therapy. Expert Opin Pharmacother 2009, 10(13):2127-2143.
- [32]Veenstra-VanderWeele J, Blakely RD: Networking in autism: leveraging genetic, biomarker and model system findings in the search for new treatments. Neuropsychopharmacol 2012, 37(1):196-212.
- [33]Woods AG, Sokolowska I, Taurines R, Gerlach M, Dudley E, Thome J, Darie CC: Potential biomarkers in psychiatry: focus on the cholesterol system. J Cell Mol Med 2012.
- [34]Dereu M, Roeyers H, Raymaekers R, Meirsschaut M, Warreyn P: How useful are screening instruments for toddlers to predict outcome at age 4? General development, language skills, and symptom severity in children with a false positive screen for autism spectrum disorder. Eur Child Adolesc Psychiatry 2012.
- [35]Junaid MA, Pullarkat RK: Proteomic approach for the elucidation of biological defects in autism. J Autism Dev Disord 2001, 31(6):557-560.
- [36]Woods AG, Sokolowska I, Yakubu R, Butkiewicz M, LaFleur M, Talbot C, Darie CC: Blue native page and mass spectrometry as an approach for the investigation of stable and transient protein-protein interactions Oxidative Stress: Diagnostics, Prevention, and Therapy. edn. Edited by Andreescu S, Hepel M. Washington, D.C.: American Chemical Society; 2011.
- [37]Anderson L, Seilhamer J: A comparison of selected mRNA and protein abundances in human liver. Electrophoresis 1997, 18(3–4):533-537.
- [38]Taurines R, Dudley E, Grassl J, Warnke A, Gerlach M, Coogan AN, Thome J: Proteomic research in psychiatry. J Psychopharmacol 2011, 25(2):151-196.
- [39]Kern JK, Grannemann BD, Trivedi MH, Adams JB: Sulfhydryl-reactive metals in autism. J Toxicol Environ Health A 2007, 70(8):715-721.
- [40]Thomas RH, Foley KA, Mepham JR, Tichenoff LJ, Possmayer F, MacFabe DF: Altered brain phospholipid and acylcarnitine profiles in propionic acid infused rodents: further development of a potential model of autism spectrum disorders. J Neurochem 2010, 113(2):515-529.
- [41]Klemmer P, Meredith RM, Holmgren CD, Klychnikov OI, Stahl-Zeng J, Loos M, van der Schors RC, Wortel J, de Wit H, Spijker S: Proteomics, ultrastructure, and physiology of hippocampal synapses in a fragile X syndrome mouse model reveal presynaptic phenotype. J Biol Chem 2011, 286(29):25495-25504.
- [42]Lista S, Faltraco F, Hampel H: Blood and plasma-based proteomic biomarker research in Alzheimer's disease. Prog Neurobiol 2012.
- [43]Amado FM, Ferreira RP, Vitorino R: One decade of salivary proteomics: Current approaches and outstanding challenges. Clin Biochem 2012.
- [44]Tambor V, Fucikova A, Lenco J, Kacerovsky M, Rehacek V, Stulik J, Pudil R: Application of proteomics in biomarker discovery: a primer for the clinician. Physiol Res 2010, 59(4):471-497.
- [45]Lovestone S, Guntert A, Hye A, Lynham S, Thambisetty M, Ward M: Proteomics of Alzheimer's disease: understanding mechanisms and seeking biomarkers. Expert Rev Proteomics 2007, 4(2):227-238.
- [46]Darie CC, Biniossek ML, Gawinowicz MA, Milgrom Y, Thumfart JO, Jovine L, Litscher ES, Wassarman PM: Mass spectrometric evidence that proteolytic processing of rainbow trout egg vitelline envelope proteins takes place on the egg. J Biol Chem 2005, 280(45):37585-37598.
- [47]Darie CC, Biniossek ML, Winter V, Mutschler B, Haehnel W: Isolation and structural characterization of the Ndh complex from mesophyll and bundle sheath chloroplasts of Zea mays. FEBS J 2005, 272(11):2705-2716.
- [48]Darie CC, Deinhardt K, Zhang G, Cardasis HS, Chao MV, Neubert TA: Identifying transient protein-protein interactions in EphB2 signaling by blue native PAGE and mass spectrometry. Proteomics 2011, 11(23):4514-4528.
- [49]Darie CC, Janssen WG, Litscher ES, Wassarman PM: Purified trout egg vitelline envelope proteins VEbeta and VEgamma polymerize into homomeric fibrils from dimers in vitro. Biochim Biophys Acta 2008, 1784(2):385-392.
- [50]Jovine L, Darie CC, Litscher ES, Wassarman PM: Zona pellucida domain proteins. Annu Rev Biochem 2005, 74:83-114.
- [51]Litscher ES, Janssen WG, Darie CC, Wassarman PM: Purified mouse egg zona pellucida glycoproteins polymerize into homomeric fibrils under non-denaturing conditions. J Cell Physiol 2008, 214(1):153-157.
- [52]Ngounou Wetie AG, Sokolowska I, Woods AG, Roy U, Loo JA, Darie CC: Investigation of stable and transient protein-protein interactions: past, present and future. Proteomics 2012.
- [53]Ngounou Wetie AG, Sokolowska I, Woods AG, Wormwood KL, Dao S, Patel S: Clarkson BD. Darie CC: Automated Mass Spectrometry-Based Functional Assay for the Routine Analysis of the Secretome. Journal of laboratory automation; 2012.
- [54]Sokolowska I, Dorobantu C, Woods AG, Macovei A, Branza-Nichita N, Darie CC: Proteomic analysis of plasma membranes isolated from undifferentiated and differentiated HepaRG cells. Proteome Sci 2012, 10(1):47. BioMed Central Full Text
- [55]Sokolowska I, Gawinowicz MA, Wetie AG, Darie CC: Disulfide proteomics for identification of extracellular or secreted proteins. Electrophoresis 2012, 33(16):2527-2536.
- [56]Sokolowska I, Ngounou Wetie AG: Woods AG. Darie CC: Automatic Determination of Disulfide Bridges in Proteins. Journal of laboratory automation; 2012.
- [57]Sokolowska I, Woods AG, Gawinowicz MA, Roy U, Darie CC: Characterization of Tumor Differentiation Factor (TDF) and its receptor (TDF-R). Cell Mol Life Sci 2012.
- [58]Spellman DS, Deinhardt K, Darie CC, Chao MV, Neubert TA: Stable isotopic labeling by amino acids in cultured primary neurons: application to brain-derived neurotrophic factor-dependent phosphotyrosine-associated signaling. Mol Cell Proteomics 2008, 7(6):1067-1076.
- [59]Woods AG, Sokolowska I, Darie CC: Identification of consistent alkylation of cysteine-less peptides in a proteomics experiment. Biochem Biophys Res Commun 2012, 419(2):305-308.
- [60]Roy U, Sokolowska I, Woods AG, Darie CC: Structural Investigation of Tumor Differentiation Factor (TDF). Biotechnol Appl Biochem 2012.
- [61]Armirotti A, Damonte G: Achievements and perspectives of top-down proteomics. Proteomics 2010, 10(20):3566-3576.
- [62]Sokolowska I, Woods AG, Wagner J, Dorler J, Wormwood K, Thome J, Darie CC: Mass spectrometry for proteomics-based investigation of oxidative stress and heat shock proteins Oxidative Stress: Diagnostics, Prevention, and Therapy. edn. Edited by Andreescu S, Hepel M. Washington, D.C.: American Chemical Society; 2011.
- [63]Lam KS, Aman MG, Arnold LE: Neurochemical correlates of autistic disorder: a review of the literature. Res Dev Disabil 2006, 27(3):254-289.
- [64]Cass H, Gringras P, March J, McKendrick I, O'Hare AE, Owen L, Pollin C: Absence of urinary opioid peptides in children with autism. Arch Dis Child 2008, 93(9):745-750.
- [65]Hunter LC, O'Hare A, Herron WJ, Fisher LA, Jones GE: Opioid peptides and dipeptidyl peptidase in autism. Dev Med Child Neurol 2003, 45(2):121-128.
- [66]Albizzati A, More L, Di Candia D, Saccani M, Lenti C: Normal concentrations of heavy metals in autistic spectrum disorders. Minerva Pediatr 2012, 64(1):27-31.
- [67]Owens SE, Summar ML, Ryckman KK, Haines JL, Reiss S, Summar SR, Aschner M: Lack of association between autism and four heavy metal regulatory genes. Neurotoxicology 2011, 32(6):769-775.
- [68]Montaser A, McLean JA, Liu H, Mermet J-M: An introduction to ICP spectrometries for elemental analysis Plasma Mass Spectrometry. edn. Edited by Montaser A. Hoboken, NJ: John Wiley & Sons; 1998.
- [69]Soden SE, Lowry JA, Garrison CB, Wasserman GS: 24-hour provoked urine excretion test for heavy metals in children with autism and typically developing controls, a pilot study. Clin Toxicol 2007, 45(5):476-481.
- [70]Emanuele E, Colombo R, Martinelli V, Brondino N, Marini M, Boso M, Barale F, Politi P: Elevated urine levels of bufotenine in patients with autistic spectrum disorders and schizophrenia. Neuro Endocrinol Lett 2010, 31(1):117-121.
- [71]McBride MC: Bufotenine: toward an understanding of possible psychoactive mechanisms. J Psychoactive Drugs 2000, 32(3):321-331.
- [72]Takeda N: Serotonin-degradative pathways in the toad (Bufo bufo japonicus) brain: clues to the pharmacological analysis of human psychiatric disorders. Comp Biochem Physiol Pharmacol Toxicol Endocrinol 1994, 107(2):275-281.
- [73]Hites RA: Gas chromatography mass spectrometry Instrumental Techniques for Analytical Chemistry. edn. Edited by Settle F. Upper Saddle River, NJ: Prentice-Hall; 1997.
- [74]Kałuzna-Czaplinska J, Michalska M, Rynkowski J: Determination of tryptophan in urine of autistic and healthy children by gas chromatography/mass spectrometry. Med Sci Monit 2010, 16(10):CR488-492.
- [75]Pedersen OS, Liu Y, Reichelt KL: Serotonin uptake stimulating peptide found in plasma of normal individuals and in some autistic urines. J Pept Res 53(6):641-646.
- [76]Yao Y, Walsh WJ, McGinnis WR, Pratico D: Altered vascular phenotype in autism: correlation with oxidative stress. Arch Neurol 2006, 63(8):1161-1164.
- [77]Taurines R, Dudley E, Conner AC, Grassl J, Jans T, Guderian F, Mehler-Wex C, Warnke A, Gerlach M, Thome J: Serum protein profiling and proteomics in autistic spectrum disorder using magnetic bead-assisted mass spectrometry. Eur Arch Psychiatry Clin Neurosci 2010, 260(3):249-255.
- [78]Corbett BA, Kantor AB, Schulman H, Walker WL, Lit L, Ashwood P, Rocke DM, Sharp FR: A proteomic study of serum from children with autism showing differential expression of apolipoproteins and complement proteins. Mol Psychiatry 2007, 12(3):292-306.
- [79]Aneja A, Tierney E: Autism: the role of cholesterol in treatment. Int Rev Psychiatry 2008, 20(2):165-170.
- [80]Tierney E, Bukelis I, Thompson RE, Ahmed K, Aneja A, Kratz L, Kelley RI: Abnormalities of cholesterol metabolism in autism spectrum disorders. Am J Med Genet 2006, 141B(6):666-668.
- [81]Hertz-Picciotto I, Croen LA, Hansen R, Jones CR, van de Water J, Pessah IN: The CHARGE study: an epidemiologic investigation of genetic and environmental factors contributing to autism. Environ Health Perspect 2006, 114(7):1119-1125.
- [82]Hertz-Picciotto I, Green PG, Delwiche L, Hansen R, Walker C, Pessah IN: Blood mercury concentrations in CHARGE Study children with and without autism. Environ Health Perspect 2010, 118(1):161-166.
- [83]Hertz-Picciotto I, Bergman A, Fangstrom B, Rose M, Krakowiak P, Pessah I, Hansen R, Bennett DH: Polybrominated diphenyl ethers in relation to autism and developmental delay: a case–control study. Environ Health-Glob 2011, 10(1):1. BioMed Central Full Text
- [84]Russo AJ, Devito R: Analysis of Copper and Zinc Plasma Concentration and the Efficacy of Zinc Therapy in Individuals with Asperger's Syndrome, Pervasive Developmental Disorder Not Otherwise Specified (PDD-NOS) and Autism. Biomarker insights 2011, 6:127-133.
- [85]Godler DE, Slater HR, Bui QM, Ono M, Gehling F, Francis D, Amor DJ, Hopper JL, Hagerman R, Loesch DZ: FMR1 intron 1 methylation predicts FMRP expression in blood of female carriers of expanded FMR1 alleles. J Mol Diagn 2011, 13(5):528-536.
- [86]Godler DE, Slater HR, Bui QM, Storey E, Ono MY, Gehling F, Inaba Y, Francis D, Hopper JL, Kinsella G: Fragile X mental retardation 1 (FMR1) intron 1 methylation in blood predicts verbal cognitive impairment in female carriers of expanded FMR1 alleles: evidence from a pilot study. Clin Chem 2012, 58(3):590-598.
- [87]Hu S, Li Y, Wang J, Xie Y, Tjon K, Wolinsky L, Loo RR, Loo JA, Wong DT: Human saliva proteome and transcriptome. J Dent Res 2006, 85:1129-1133.
- [88]Wiesen MH, Farowski F, Feldkotter M, Hoppe B, Muller C: Liquid chromatography-tandem mass spectrometry method for the quantification of mycophenolic acid and its phenolic glucuronide in saliva and plasma using a standardized saliva collection device. J Chromatogr A 2012, 1241:52-59.
- [89]Border MB, Schwartz S, Carlson J, Dibble CF, Kohltfarber H, Offenbacher S, Buse JB, Bencharit S: Exploring salivary proteomes in edentulous patients with type 2 diabetes. Mol Biosyst 2012, 8(4):1304-1310.
- [90]Shi M, Sui YT, Peskind ER, Li G, Hwang H, Devic I, Ginghina C, Edgar JS, Pan C, Goodlett DR: Salivary tau species are potential biomarkers of Alzheimer's disease. J Alzheimers Dis 2011, 27(2):299-305.
- [91]Soukup M, Biesiada I, Henderson A, Idowu B, Rodeback D, Ridpath L, Bridges EG, Nazar AM, Bridges KG: Salivary uric acid as a noninvasive biomarker of metabolic syndrome. Diab Metab Synd 2012, 4(1):14. BioMed Central Full Text
- [92]Castagnola M, Messana I, Inzitari R, Fanali C, Cabras T, Morelli A, Pecoraro AM, Neri G, Torrioli MG, Gurrieri F: Hypo-phosphorylation of salivary peptidome as a clue to the molecular pathogenesis of autism spectrum disorders. J Proteome Res 2008, 7(12):5327-5332.
- [93]Sokolowska I, Woods AG, Gawinowicz MA, Roy U, Darie CC: Identification of a potential tumor differentiation factor receptor candidate in prostate cancer cells. FEBS J 2012, 279(14):2579-2594.
- [94]Sokolowska I, Woods AG, Gawinowicz MA, Roy U, Darie CC: Identification of potential tumor differentiation factor (TDF) receptor from steroid-responsive and steroid-resistant breast cancer cells. J Biol Chem 2012, 287(3):1719-1733.
- [95]Darie CC, Shetty V, Spellman DS, Zhang G, Xu C, Cardasis HL, Blais S, Fenyo D, Neubert T: A.: Blue Native PAGE and mass spectrometry analysis of the ephrin stimulation- dependent protein-protein interactions in NG108-EphB2 cells. Düsseldorf, Germany: Springer; 2008.
- [96]Darie CC, Biniossek ML, Jovine L, Litscher ES, Wassarman PM: Structural characterization of fish egg vitelline envelope proteins by mass spectrometry. Biochemistry 2004, 43(23):7459-7478.
- [97]Darie CC, Litscher ES, Wassarman PM: Structure, processing, and polymerization of rainbow trout egg vitelline envelope proteins. Düsseldorf, Germany: Springer; 2008.
- [98]Godler DE, Tassone F, Loesch DZ, Taylor AK, Gehling F, Hagerman RJ, Burgess T, Ganesamoorthy D, Hennerich D, Gordon L: Methylation of novel markers of fragile X alleles is inversely correlated with FMRP expression and FMR1 activation ratio. Hum Mol Genet 2010, 19(8):1618-1632.
PDF