Serum proteomic analysis identifies sex-specific differences in lipid metabolism and inflammation profiles in adults diagnosed with Asperger syndrome

Molecular Autism

Volumn 5, Issue 1, 2014, Pages

  Steeb, Hannah ^a   Ramsey, Jordan M ^a   Guest, Paul C ^a   Stocki, Pawel ^a   Cooper, Jason D ^a   Rahmoune, Hassan ^a   Ingudomnukul, Erin ^b   Auyeung, Bonnie ^b   Ruta, Liliana ^c   Baron Cohen, Simon ^b   Bahn, Sabine ^a,d  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c DEPARTMENT OF DEVELOPMENTAL NEUROSCIENCE   (Italy)

^d ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Asperger Syndrome; Biomarkers; Growth; Inflammation; Lipid transport; Proteomics; Sex

Indexed keywords

ADIPONECTIN; APOLIPOPROTEIN E; ARMC3 PROTEIN; BONE MORPHOGENETIC PROTEIN 6; CHROMOGRANIN A; CLC4K PROTEIN; CONNECTIVE TISSUE GROWTH FACTOR; EOTAXIN 3; EPIDERMAL GROWTH FACTOR; ERYTHROPOIETIN; FATTY ACID BINDING PROTEIN; FERRITIN; FETUB PROTEIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN M; INTERLEUKIN 12P70; INTERLEUKIN 16; INTERLEUKIN 3; MRRP1 PROTEIN; PROTEIN; PTPA PROTEIN; RN149 PROTEIN; SEX HORMONE BINDING GLOBULIN; TENASCIN; THROMBOPLASTIN; TLE1 PROTEIN; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TRIPB PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ZC3HE PROTEIN;

ADULT; ALCOHOL CONSUMPTION; ARTICLE; ASPERGER SYNDROME; BODY MASS; CLINICAL ARTICLE; CONTROLLED STUDY; EXERCISE; FEMALE; HUMAN; IMMUNOASSAY; INFLAMMATION; LIPID METABOLISM; LIPID TRANSPORT; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; ORAL CONTRACEPTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SMOKING;

EID: 84893342274     PISSN: None     EISSN: 20402392     Source Type: Journal    
DOI: 10.1186/2040-2392-5-4     Document Type: Article

References (65)

1. American Psychiatric Association, Diagnostic and Statistical Manual of Mental Disorders IV Washington DC: American Psychiatric Press Inc 1994 ISBN-10: 0890420262
2. Prevalence of autism-spectrum conditions: UK school-based population study. Baron-Cohen S, Scott FJ, Allison C, Williams J, Bolton P, Matthews FE, Brayne C, Br J Psychiatry 2009 194 500 509 10.1192/bjp.bp.108.059345 19478287
3. Prevalence of disorders of the autism spectrum in a population cohort of children in South Thames: the Special Needs and Autism Project (SNAP). Baird G, Simonoff E, Pickles A, Chandler S, Loucas T, Meldrum D, Charman T, Lancet 2006 368 210 215 10.1016/S0140-6736(06)69041-7 16844490 (Pubitemid 44037796)
4. Asperger syndrome. Woodbury-Smith MR, Volkmar FR, Eur Child Adolesc Psychiatry 2009 18 2 11 10.1007/s00787-008-0701-0 18563474
5. An epidemiological and diagnostic study of Asperger syndrome according to four sets of diagnostic criteria. Mattila ML, Kielinen M, Jussila K, Linna SL, Bloigu R, Ebeling H, Moilanen I, J Am Acad Child Adolesc Psychiatry 2007 46 636 646 10.1097/chi.0b013e318033ff42 17450055 (Pubitemid 46642581)
6. Sex-specific serum biomarker patterns in adults with Asperger's syndrome. Schwarz E, Guest PC, Rahmoune H, Wang L, Levin Y, Ingudomnukul E, Ruta L, Kent L, Spain M, Baron-Cohen S, Bahn S, Mol Psychiatry 2011 16 1213 1220 10.1038/mp.2010.102 20877284
7. Molecular sex differences in human serum. Ramsey JM, Schwarz E, Guest PC, van Beveren NJ, Leweke FM, Rothermundt M, Bogerts B, Steiner J, Ruta L, Baron-Cohen S, Bahn S, PLoS One 2012 7 51504 10.1371/journal.pone.0051504 23251558
8. Care of the patient with an autism spectrum disorder by the general physician. Venkat A, Jauch E, Russell WS, Crist CR, Farrell R, Postgrad Med J 2012 88 472 481 10.1136/postgradmedj-2011-130727 22427366
9. Quantification of proteins using data-independent analysis (MSE) in simple andcomplex samples: a systematic evaluation. Levin Y, Hradetzky E, Bahn S, Proteomics 2011 11 3273 3287 10.1002/pmic.201000661 21751355
10. The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E, J Autism Dev Disord 2001 31 5 17 10.1023/A:1005653411471 11439754
11. Identification of a biological signature for schizophrenia in serum. Schwarz E, Guest PC, Rahmoune H, Harris LW, Wang L, Leweke FM, Rothermundt M, Bogerts B, Koethe D, Kranaster L, Ohrmann P, Suslow T, McAllister G, Spain M, Barnes A, van Beveren NJ, Baron-Cohen S, Steiner J, Torrey FE, Yolken RH, Bahn S, Mol Psychiatry 2012 17 494 502 10.1038/mp.2011.42 21483431
12. Database searching and accounting of multiplexed precursor and product ion spectra from the data independent analysis of simple and complex peptide mixtures. Li GZ, Vissers JP, Silva JC, Golick D, Gorenstein MV, Geromanos SJ, Proteomics 2009 9 1696 1719 10.1002/pmic.200800564 19294629
13. Label-free detection of differential protein expression by LC/MALDI mass spectrometry. Neubert H, Bonnert TP, Rumpel K, Hunt BT, Henle ES, James IT, J Proteome Res 2008 7 2270 2279 10.1021/pr700705u 18412385
14. The application of selective reaction monitoring confirms dysregulation of glycolysis in a preclinical model of schizophrenia. Martins-de-Souza D, Alsaif M, Ernst A, Harris LW, Aerts N, Lenaerts I, Peeters PJ, Amess B, Rahmoune H, Bahn S, Guest PC, BMC research notes 2012 5 146 10.1186/1756-0500-5-146 22420779
15. Protein significance analysis in selected reaction monitoring (SRM) measurements. Chang CY, Picotti P, Hüttenhain R, Heinzelmann-Schwarz V, Jovanovic M, Aebersold R, Vitek O, Mol Cell Proteomics 2012 11 4 111.014662 10.1074/mcp.M111.014662. [Epub21 Dec 2011]. 22190732
16. Elevated rates of testosterone-related disorders in women with autism spectrum conditions. Ingudomnukul E, Baron-Cohen S, Wheelwright S, Knickmeyer R, Horm Behav 2007 51 597 604 10.1016/j.yhbeh.2007.02.001 17462645 (Pubitemid 46770756)
17. Cell adhesion molecules and their involvement in autism spectrum disorder. Ye H, Liu J, Wu JY, Neurosignals 2010 18 62 71 10.1159/000322543 21212702
18. Urinary cortisol circadian rhythm in a group of high-functioning children with autism. Richdale AL, Prior MR, J Autism Dev Disord 1992 22 433 447 10.1007/BF01048245 1400105
19. Proinflammatory and regulatory cytokine production associated with innate and adaptive immune responses in children with autism spectrum disorders and developmental regression. Jyonouchi H, Sun S, Le H, J Neuroimmunol 2001 120 170 179 10.1016/S0165-5728(01)00421-0 11694332 (Pubitemid 33016737)
20. Serum neurotrophin concentrations in autism and mental retardation: a pilot study. Miyazaki K, Narita N, Sakuta R, Miyahara T, Naruse H, Okado N, Narita M, Brain Dev 2004 26 292 295 10.1016/S0387-7604(03)00168-2 15165668 (Pubitemid 38692430)
21. Plasma cytokine profiles in subjects with high-functioning autism spectrum disorders. Suzuki K, Matsuzaki H, Iwata K, Kameno Y, Shimmura C, Kawai S, Yoshihara Y, Wakuda T, Takebayashi K, Takagai S, Matsumoto K, Tsuchiya KJ, Iwata Y, Nakamura K, Tsujii M, Sugiyama T, Mori N, PLoS One 2011 6 20470 10.1371/journal.pone.0020470 21647375
22. Associations of impaired behaviours with elevated plasma chemokines in autism spectrum disorders. Ashwood P, Krakowiak P, Hertz-Picciotto I, Hansen R, Pessah IN, Van de Water J, J Neuroimmunol 2011 232 196 199 10.1016/j.jneuroim. 2010.10.025 21095018
23. Reduced levels of immunoglobulin in children with autism correlates with behavioral symptoms. Heuer L, Ashwood P, Schauer J, Goines P, Krakowiak P, Hertz-Picciotto I, Hansen R, Croen LA, Pessah IN, Van de Water J, Autism Res 2008 1 275 283 10.1002/aur.42 19343198
24. Ferritin and iron levels in children with autistic disorder. Hergüner S, Keleşoǧlu FM, Tanidir C, Cöpür M, Eur J Pediatr 2012 171 143 146 10.1007/s00431-011-1506-6 21643649
25. Investigation of the serum levels of anterior pituitary hormones in male children with autism. Iwata K, Matsuzaki H, Miyachi T, Shimmura C, Suda S, Tsuchiya KJ, Matsumoto K, Suzuki K, Iwata Y, Nakamura K, Tsujii M, Sugiyama T, Sato K, Mori N, Mol Autism 2011 2 16 doi:10.1186/2040-2392-2-16 10.1186/2040-2392-2-16 22011527
26. Abnormalities of cholesterol metabolism in autism spectrum disorders. Tierney E, Bukelis I, Thompson RE, Ahmed K, Aneja A, Kratz L, Kelley RI, Am J Med Genet B Neuropsychiatr Genet 2006 141B 666 668 10.1002/ajmg.b.30368 16874769 (Pubitemid 44434669)
27. Metabolic profiles in adults with autism spectrum disorder and intellectual disabilities. Moses L, Katz N, Weizman A, Eur Psychiatry 2013 10.1016/j.eurpsy.2013.05.005. [Epub ahead of print]
28. Potential biomarkers in psychiatry: focus on the cholesterol system. Woods AG, Sokolowska I, Taurines R, Gerlach M, Dudley E, Thome J, Darie CC, J Cell Mol Med 2012 16 1184 1195 10.1111/j.1582-4934.2012.01543.x 22304330
29. Autism: the role of cholesterol in treatment. Aneja A, Tierney E, Int Rev Psychiatry 2008 20 165 170 10.1080/09540260801889062 18386207 (Pubitemid 351489516)
30. Pervasive developmental disorders in children of hyperandrogenic women with polycystic ovary syndrome: a longitudinal case-control study. Palomba S, Marotta R, Di Cello A, Russo T, Falbo A, Orio F, Tolino A, Zullo F, Esposito R, La Sala GB, Clin Endocrinol (Oxf) 2012 77 898 904 10.1111/j.1365-2265.2012. 04443.x 22612600
31. Control of energy homeostasis and insulin action by adipocyte hormones: leptin, acylation stimulating protein, and adiponectin. Havel PJ, Curr Opin Lipidol 2002 13 51 59 10.1097/00041433-200202000-00008 11790963 (Pubitemid 34174629)
32. Glucuronic acid epimerase is associated with plasma triglyceride and high-density lipoprotein cholesterol levels in Turks. Hodoǧlugil U, Williamson DW, Yu Y, Farrer LA, Mahley RW, Ann Hum Genet 2011 75 398 417 10.1111/j.1469-1809.2011.00644.x 21488854
33. Downregulation of fetuin-B and zinc-α2-glycoprotein is linked to impaired fatty acid metabolism in liver cells. Choi JW, Liu H, Mukherjee R, Yun JW, Cell Physiol Biochem 2012 30 295 306 10.1159/000339065 22739111
34. Role of sex steroids, intrahepatic fat and liver enzymes in the association between SHBG and metabolic features. Bonnet F, Cephise FL, Gautier A, Dubois S, Massart C, Camara A, Larifla L, Balkau B, Ducluzeau PH, Clin Endocrinol (Oxf) 2012 79 517 522 [Epub ahead of print]
35. Sex hormone-binding globulin: anatomy and physiology of a new regulatory system. Rosner W, Hryb DJ, Khan MS, Nakhla AM, Romas NA, J Steroid Biochem Mol Biol 1991 40 813 820 10.1016/0960-0760(91)90307-Q 1659894
36. Fetal testosterone and autistic traits. Auyeung B, Baron-Cohen S, Ashwin E, Knickmeyer R, Taylor K, Hackett G, Br J Psychol 2009 100 1 22 10.1348/000712608X311731 18547459
37. The effect of statins on testosterone in men and women, a systematic review and meta-analysis of randomized controlled trials. Schooling CM, Au Yeung SL, Freeman G, Cowling BJ, BMC Med 2013 11 57 10.1186/1741-7015-11-57 23448151
38. The effect of atorvastatin in patients with polycystic ovary syndrome: a randomized double-blind placebo-controlled study. Sathyapalan T, Kilpatrick ES, Coady AM, Atkin SL, J Clin Endocrinol Metab 2009 94 103 108 10.1210/jc.2008-1750 18940877
39. Effects of simvastatin and oral contraceptive agent on polycystic ovary syndrome: prospective, randomised, crossover trial. Banaszewska B, Pawelczyk L, Spaczynski RZ, Dziura J, Duleba AJ, J Clin Endocrinol Metab 2007 92 456 461 Epub 2006 Nov 14 10.1210/jc.2006-1988 17105841
40. May lovastatin target both autism and epilepsy? A novel hypothesized treatment. Ghanizadeh A, Epilepsy Behav 2011 20 422 10.1016/j.yebeh.2010.12.027 21269887
41. Effects of insulin-sensitizing agents and insulin resistance in women with polycystic ovary syndrome. Hwang KR, Choi YM, Kim JJ, Chae SJ, Park KE, Jeon HW, Ku SY, Kim SH, Kim JG, Moon SY, Clin Exp Reprod Med 2013 40 100 105 10.5653/cerm.2013.40.2.100 23875167
42. Biomarkers in neuroendocrine tumors. Chromogranin A, Duque M, Modlin IM, Gupta A, Saif MW, JOP 2013 14 372 376 23846930
43. Erythropoietin and IL-3 induce tyrosine phosphorylation of CrkL and its association with Shc, SHP-2, and Cbl in hematopoietic cells. Chin H, Saito T, Arai A, Yamamoto K, Kamiyama R, Miyasaka N, Miura O, Biochem Biophys Res Commun 1997 239 412 417 10.1006/bbrc.1997.7480 9344843 (Pubitemid 27488977)
44. Prostate cancer-associated markers. Chu TM, Immunol Ser 1990 53 339 356 1713065
45. Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Janssens V, Goris J, Biochem J 2001 353 417 439 10.1042/0264-6021:3530417 11171037 (Pubitemid 32158309)
46. Transducin-like enhancer of Split-1 (TLE1) combines with Forkhead box protein G1 (FoxG1) to promote neuronal survival. Dastidar SG, Narayanan S, Stifani S, D'Mello SR, J Biol Chem 2012 287 14749 14759 10.1074/jbc.M111.328336 22354967
47. Ring finger protein 149 is an E3 ubiquitin ligase active on wild-type v-Raf murine sarcoma viral oncogene homolog B1 (BRAF). Hong SW, Jin DH, Shin JS, Moon JH, Na YS, Jung KA, Kim SM, Kim JC, Kim KP, Hong YS, Lee JL, Choi EK, Lee JS, Kim TW, J Biol Chem 2012 287 24017 24025 10.1074/jbc.M111.319822 22628551
48. Lethal skeletal dysplasia in mice and humans lacking the golgin GMAP-210. Smits P, Bolton AD, Funari V, Hong M, Boyden ED, Lu L, Manning DK, Dwyer ND, Moran JL, Prysak M, Merriman B, Nelson SF, Bonafé L, Superti-Furga A, Ikegawa S, Krakow D, Cohn DH, Kirchhausen T, Warman ML, Beier DR, N Engl J Med 2010 362 206 216 10.1056/NEJMoa0900158 20089971
49. Brief report: immunoglobulin A deficiency in a subset of autistic subjects. Warren RP, Odell JD, Warren WL, Burger RA, Maciulis A, Daniels WW, Torres AR, J Autism Dev Disord 1997 27 187 192 10.1023/A:1025895925178 9105969 (Pubitemid 27157493)
50. Increased expression of tenascin C by keloids in vivo and in vitro. Dalkowski A, Schuppan D, Orfanos CE, Zouboulis CC, Br J Dermatol 1999 141 50 56 10.1046/j.1365-2133.1999.02920.x 10417515 (Pubitemid 29333693)
51. New kid on the ID block: neural functions of the Nab2/ZC3H14 class of CysHis tandem zinc-finger polyadenosine RNA binding proteins. Kelly S, Pak C, Garshasbi M, Kuss A, Corbett AH, Moberg K, RNA Biol 2012 9 555 562 10.4161/rna.20187 22614829
52. Unexpected expansion of tRNA substrate recognition by the yeast m1G9 methyltransferase Trm10. Swinehart WE, Henderson JC, Jackman JE, RNA 2013 19 1137 1146 10.1261/rna.039651.113 23793893
53. Cloning and expression of ARMC3-v2, a novel splicing variant of the human ARMC3 gene. Li X, Liu B, Ji CN, Kang Y, Mao Y, Genetika 2006 42 999 1003 16915934
54. Activation of the inflammatory response system in autism. Croonenberghs J, Bosmans E, Deboutte D, Kenis G, Maes M, Neuropsychobiology 2002 45 1 6 11803234 (Pubitemid 34117721)
55. Serum levels of soluble platelet endothelial cell adhesion molecule-1 and vascular cell adhesion molecule-1 are decreased in subjects with autism spectrum disorder. Kameno Y, Iwata K, Matsuzaki H, Miyachi T, Tsuchiya KJ, Matsumoto K, Iwata Y, Suzuki K, Nakamura K, Maekawa M, Tsujii M, Sugiyama T, Mori N, Mol Autism 2013 4 19 10.1186/2040-2392-4-19 23773279
56. Tissue factor signalling: a multi-faceted function in biological processes. van den Hengel LG, Versteeg HH, Front Biosci (Schol Ed) 2011 3 1500 1510 21622285
57. Connective tissue growth factor (CTGF/CCN2) ELISA: a novel tool for monitoring fibrosis. Dendooven A, Gerritsen KG, Nguyen TQ, Kok RJ, Goldschmeding R, Biomarkers 2011 16 289 301 10.3109/1354750X.2011.561366 21595567
58. Plasma increase of interleukin-12 and interferon-gamma. Pathological significance in autism. Singh VK, J Neuroimmunol 1996 66 143 145 10.1016/0165-5728(96)00014-8 8964908 (Pubitemid 26193945)
59. An open-label pilot study of a formulation containing the anti-inflammatory flavonoid luteolin and its effects on behavior in children with autism spectrum disorders. Taliou A, Zintzaras E, Lykouras L, Francis K, Clin Ther 2013 35 592 602 10.1016/j.clinthera.2013.04.006 23688534
60. Celecoxib as adjunctive treatment to risperidone in children with autistic disorder: a randomized, double-blind, placebo-controlled trial. Asadabadi M, Mohammadi MR, Ghanizadeh A, Modabbernia A, Ashrafi M, Hassanzadeh E, Forghani S, Akhondzadeh S, Psychopharmacology (Berl) 2013 225 51 59 10.1007/s00213-012-2796-8 22782459
61. BMP2 and BMP6 control p57(Kip2) expression and cell growth arrest/terminal differentiation in normal primary human epidermal keratinocytes. Gosselet FP, Magnaldo T, Culerrier RM, Sarasin A, Ehrhart JC, Cell Signal 2007 19 731 739 10.1016/j.cellsig.2006.09.006 17112701 (Pubitemid 46275366)
62. Arfaptins are localized to the trans-Golgi by interaction with Arl1, but not Arfs. Man Z, Kondo Y, Koga H, Umino H, Nakayama K, Shin HW, J Biol Chem 2011 286 11569 11578 10.1074/jbc.M110.201442 21239483
63. A behavioural comparison of male and female adults with high functioning autism spectrum conditions. Lai MC, Lombardo MV, Pasco G, Ruigrok AN, Wheelwright SJ, Sadek SA, Chakrabarti B, Baron-Cohen S, MRC AIMS Consortium, PLoS One 2011 6 20835 10.1371/journal.pone.0020835 21695147
64. Biological sex affects the neurobiology of autism. Lai MC, Lombardo MV, Suckling J, Ruigrok AN, Chakrabarti B, Ecker C, Deoni SC, Craig MC, Murphy DG, Bullmore ET, Baron-Cohen S, MRC AIMS Consortium, Brain 2013 136 2799 2815 10.1093/brain/awt216 23935125
65. Why are autism spectrum conditions more prevalent in males? Baron-Cohen S, Lombardo MV, Auyeung B, Ashwin E, Chakrabarti B, Knickmeyer R, PLoS Biol 2011 9 1001081 10.1371/journal.pbio.1001081 21695109