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Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Mini-Review Article

Autism Spectrum Disorders: Advances in Proteomics

Author(s): Hui Zhou and Xiao-Li Feng*

Volume 30, Issue 5, 2023

Published on: 10 May, 2023

Page: [384 - 395] Pages: 12

DOI: 10.2174/0929866530666230411122644

Price: $65

Abstract

Autism is a class of developmental disorders with extremely high rates of disability, affecting patients throughout their lives. There is no cure to date clinically, and early rehabilitation interventions can improve some of the behavioral problems of autistic patients, but these are limited by age and often have minimal effects in older adults with autism. Early diagnosis is also necessary while developing effective autism therapies. At present, the early diagnosis of autism is dependent on the search for effective markers in an attempt to screen differentially expressed proteins in autistic patients using high-throughput assays, such as synaptic scaffolding proteins, microtubule-associated proteins, apolipoproteins, immunoglobulin G complement factor-related proteins, etc. It would also be a big step forward for mechanistic studies of autism if a valid biomarker for autism could be found.

Graphical Abstract

[1]
Taylor, M.J.; Rosenqvist, M.A.; Larsson, H.; Gillberg, C.; D’Onofrio, B.M.; Lichtenstein, P.; Lundström, S. Etiology of autism spectrum disorders and autistic traits over time. JAMA Psychiatry, 2020, 77(9), 936-943.
[http://dx.doi.org/10.1001/jamapsychiatry.2020.0680] [PMID: 32374377]
[2]
Junaid, M.A.; Kowal, D.; Barua, M.; Pullarkat, P.S.; Sklower Brooks, S.; Pullarkat, R.K. Proteomic studies identified a single nucleotide polymorphism in glyoxalase I as autism susceptibility factor. Am. J. Med. Genet., 2004, 131A(1), 11-17.
[http://dx.doi.org/10.1002/ajmg.a.30349] [PMID: 15386471]
[3]
Doherty, M.; Haydon, C.; Davidson, I.A. Recognising autism in healthcare. Br. J. Hosp. Med., 2021, 82(12), 1-7.
[http://dx.doi.org/10.12968/hmed.2021.0313] [PMID: 34983217]
[4]
Santangelo, S.L.; Tsatsanis, K. What is known about autism: Genes, brain, and behavior. Am. J. Pharmacogen, 2005, 5(2), 71-92.
[http://dx.doi.org/10.2165/00129785-200505020-00001] [PMID: 15813671]
[5]
Pichitpunpong, C.; Thongkorn, S.; Kanlayaprasit, S.; Yuwattana, W.; Plaingam, W.; Sangsuthum, S.; Aizat, W.M.; Baharum, S.N.; Tencomnao, T.; Hu, V.W.; Sarachana, T. Phenotypic subgrouping and multi-omics analyses reveal reduced diazepam-binding inhibitor (DBI) protein levels in autism spectrum disorder with severe language impairment. PLoS One, 2019, 14(3), e0214198.
[http://dx.doi.org/10.1371/journal.pone.0214198] [PMID: 30921354]
[6]
Ferrari, A.J.; Santomauro, D.F.; Herrera, A.M.M.; Shadid, J.; Ashbaugh, C.; Erskine, H.E.; Charlson, F.J.; Degenhardt, L.; Scott, J.G.; McGrath, J.J.; Allebeck, P.; Benjet, C.; Breitborde, N.J.K.; Brugha, T.; Dai, X.; Dandona, L.; Dandona, R.; Fischer, F.; Haagsma, J.A.; Maria Haro, J.; Kieling, C.; Knudsen, A.K.S.; Kumar, G.A.; Leung, J.; Majeed, A.; Mitchell, P.B.; Moitra, M.; Mokdad, A.H.; Molokhia, M.; Patten, S.B.; Patton, G.C.; Phillips, M.R.; Soriano, J.B.; Stein, D.J.; Stein, M.B.; Szoeke, C.E.I.; Naghavi, M.; Hay, S.I.; Murray, C.J.L.; Vos, T.; Whiteford, H.A.; Collabor, G.B.D.M.D. Global, regional, and national burden of 12 mental disorders in 204 countries and territories, 1990–2019: A systematic analysis for the global burden of disease study 2019. Lancet Psychiatry, 2022, 9(2), 137-150.
[http://dx.doi.org/10.1016/S2215-0366(21)00395-3] [PMID: 35026139]
[7]
Whitehouse, A.J.O.; Varcin, K.J.; Pillar, S.; Billingham, W.; Alvares, G.A.; Barbaro, J.; Bent, C.A.; Blenkley, D.; Boutrus, M.; Chee, A.; Chetcuti, L.; Clark, A.; Davidson, E.; Dimov, S.; Dissanayake, C.; Doyle, J.; Grant, M.; Green, C.C.; Harrap, M.; Iacono, T.; Matys, L.; Maybery, M.; Pope, D.F.; Renton, M.; Rowbottam, C.; Sadka, N.; Segal, L.; Slonims, V.; Smith, J.; Taylor, C.; Wakeling, S.; Wan, M.W.; Wray, J.; Cooper, M.N.; Green, J.; Hudry, K. Effect of preemptive intervention on developmental outcomes among infants showing early signs of autism. JAMA Pediatr., 2021, 175(11), e213298.
[http://dx.doi.org/10.1001/jamapediatrics.2021.3298] [PMID: 34542577]
[8]
Thi Vui, L.; Duc, D.M.; Thuy Quynh, N.; Giang, N.T.H.; Mai, V.T.T.; Ha, B.T.T.; Van Minh, H. Early screening and diagnosis of autism spectrum disorders in Vietnam: A population-based cross-sectional survey. J. Public Health Res., 2021, 11(2), 2460.
[PMID: 34850618]
[9]
Johnson, C.P.; Myers, S.M. Identification and evaluation of children with autism spectrum disorders. Pediatrics, 2007, 120(5), 1183-1215.
[http://dx.doi.org/10.1542/peds.2007-2361] [PMID: 17967920]
[10]
Hadders-Algra, M. Early diagnostics and early intervention in neurodevelopmental disorders-age-dependent challenges and opportunities. J. Clin. Med., 2021, 10(4), 861.
[http://dx.doi.org/10.3390/jcm10040861] [PMID: 33669727]
[11]
Panerai, S.; Zingale, M.; Trubia, G.; Finocchiaro, M.; Zuccarello, R.; Ferri, R.; Elia, M. Special education versus inclusive education: the role of the TEACCH program. J. Autism Dev. Disord., 2009, 39(6), 874-882.
[http://dx.doi.org/10.1007/s10803-009-0696-5] [PMID: 19205860]
[12]
Tsang, S.K.M.; Shek, D.T.L.; Lam, L.L.; Tang, F.L.Y.; Cheung, P.M.P. Brief report: Application of the TEACCH program on Chinese pre-school children with autism-Does culture make a difference? J. Autism Dev. Disord., 2007, 37(2), 390-396.
[http://dx.doi.org/10.1007/s10803-006-0199-6] [PMID: 16906461]
[13]
Palazzi, A.; Filippa, M.; Meschini, R.; Piccinini, C.A. Music therapy enhances preterm infant’s signs of engagement and sustains maternal singing in the NICU. Infant Behav. Dev., 2021, 64, 101596.
[http://dx.doi.org/10.1016/j.infbeh.2021.101596] [PMID: 34118653]
[14]
Filippa, M.; Nardelli, M.; Della Casa, E.; Berardi, A.; Picciolini, O.; Meloni, S.; Lunardi, C.; Cecchi, A.; Sansavini, A.; Corvaglia, L.; Scilingo, E.P.; Ferrari, F.; Grp, E.V.C. Maternal singing but not speech enhances vagal activity in preterm infants during hospitalization: Preliminary results. Children, 2022, 9(2), 140.
[http://dx.doi.org/10.3390/children9020140] [PMID: 35204861]
[15]
Zhang, Y.; Liu, X.; Guo, R.; Xu, W.; Guo, Q.; Hao, C.; Ni, X.; Li, W. Biological implications of genetic variations in autism spectrum disorders from genomics studies. Biosci. Rep., 2021, 41(7), BSR20210593.
[http://dx.doi.org/10.1042/BSR20210593] [PMID: 34240107]
[16]
Ní Ghrálaigh, F.; Gallagher, L.; Lopez, L.M. Autism spectrum disorder genomics: The progress and potential of genomic technologies. Genomics, 2020, 112(6), 5136-5142.
[http://dx.doi.org/10.1016/j.ygeno.2020.09.022] [PMID: 32941983]
[17]
Abreu, A.C.; Navas, M.M.; Fernández, C.P.; Sánchez-Santed, F.; Fernández, I. NMR-based metabolomics approach to explore brain metabolic changes induced by prenatal exposure to autism-inducing chemicals. ACS Chem. Biol., 2021, 16(4), 753-765.
[http://dx.doi.org/10.1021/acschembio.1c00053] [PMID: 33728896]
[18]
Al-Ayadhi, L.; Halepoto, D.M. Role of proteomics in the discovery of autism biomarkers. J. Coll. Physicians Surg. Pak., 2013, 23(2), 137-143.
[PMID: 23374519]
[19]
Yang, J.; Chen, Y.; Xiong, X.; Zhou, X.; Han, L.; Ni, L.; Wang, W.; Wang, X.; Zhao, L.; Shao, D.; Huang, C. Peptidome analysis reveals novel serum biomarkers for children with autism spectrum disorder in China. Proteomics Clin. Appl., 2018, 12(5), 1700164.
[http://dx.doi.org/10.1002/prca.201700164] [PMID: 29754444]
[20]
Ristori, M.V.; Mortera, S.L.; Marzano, V.; Guerrera, S.; Vernocchi, P.; Ianiro, G.; Gardini, S.; Torre, G.; Valeri, G.; Vicari, S.; Gasbarrini, A.; Putignani, L. Proteomics and metabolomics approaches towards a functional insight onto autism spectrum disorders: Phenotype stratification and biomarker discovery. Int. J. Mol. Sci., 2020, 21(17), 6274.
[http://dx.doi.org/10.3390/ijms21176274] [PMID: 32872562]
[21]
Castagnola, M.; Messana, I.; Inzitari, R.; Fanali, C.; Cabras, T.; Morelli, A.; Pecoraro, A.M.; Neri, G.; Torrioli, M.G.; 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.
[http://dx.doi.org/10.1021/pr8004088] [PMID: 19367726]
[22]
Jin, C.; Kim, S.; Kang, H.; Yun, K.N.; Lee, Y.; Zhang, Y.; Kim, Y.; Kim, J.Y.; Han, K. Shank3 regulates striatal synaptic abundance of Cyld, a deubiquitinase specific for Lys63‐linked polyubiquitin chains. J. Neurochem., 2019, 150(6), 776-786.
[http://dx.doi.org/10.1111/jnc.14796] [PMID: 31215654]
[23]
Monteiro, P.; Feng, G. SHANK proteins: Roles at the synapse and in autism spectrum disorder. Nat. Rev. Neurosci., 2017, 18(3), 147-157.
[http://dx.doi.org/10.1038/nrn.2016.183] [PMID: 28179641]
[24]
Wu, S.H.; Li, X.; Qin, D.D.; Zhang, L.H.; Cheng, T.L.; Chen, Z.F.; Nie, B.B.; Ren, X.F.; Wu, J.; Wang, W.C.; Hu, Y.Z.; Gu, Y.L.; Lv, L.B.; Yin, Y.; Hu, X.T.; Qiu, Z.L. Induction of core symptoms of autism spectrum disorder by in vivo CRISPR/Cas9-based gene editing in the brain of adolescent rhesus monkeys. Sci. Bull., 2021, 66(9), 937-946.
[http://dx.doi.org/10.1016/j.scib.2020.12.017] [PMID: 36654241]
[25]
D’Incal, C.; Broos, J.; Torfs, T.; Kooy, R.F.; Vanden Berghe, W. Towards kinase inhibitor therapies for fragile X syndrome: Tweaking twists in the autism spectrum kinase signaling network. Cells, 2022, 11(8), 1325.
[http://dx.doi.org/10.3390/cells11081325] [PMID: 35456004]
[26]
Cast, T.P.; Boesch, D.J.; Smyth, K.; Shaw, A.E.; Ghebrial, M.; Chanda, S. An autism-associated mutation impairs neuroligin-4 glycosylation and enhances excitatory synaptic transmission in human neurons. J. Neurosci., 2021, 41(3), 392-407.
[http://dx.doi.org/10.1523/JNEUROSCI.0404-20.2020] [PMID: 33268543]
[27]
Kim, S.; Kim, Y.E.; Song, I.; Ujihara, Y.; Kim, N.; Jiang, Y.H.; Yin, H.H.; Lee, T.H.; Kim, I.H. Neural circuit pathology driven by Shank3 mutation disrupts social behaviors. Cell Rep., 2022, 39(10), 110906.
[http://dx.doi.org/10.1016/j.celrep.2022.110906] [PMID: 35675770]
[28]
Yuen, R.K.C.; Thiruvahindrapuram, B.; Merico, D.; Walker, S.; Tammimies, K.; Hoang, N.; Chrysler, C.; Nalpathamkalam, T.; Pellecchia, G.; Liu, Y.; Gazzellone, M.J.; D’Abate, L.; Deneault, E.; Howe, J.L.; Liu, R.S.C.; Thompson, A.; Zarrei, M.; Uddin, M.; Marshall, C.R.; Ring, R.H.; Zwaigenbaum, L.; Ray, P.N.; Weksberg, R.; Carter, M.T.; Fernandez, B.A.; Roberts, W.; Szatmari, P.; Scherer, S.W. Whole-genome sequencing of quartet families with autism spectrum disorder. Nat. Med., 2015, 21(2), 185-191.
[http://dx.doi.org/10.1038/nm.3792] [PMID: 25621899]
[29]
Bailey, A.; Phillips, W.; Rutter, M. Autism: towards an integration of clinical, genetic, neuropsychological, and neurobiological perspectives. J. Child Psychol. Psychiatry, 1996, 37(1), 89-126.
[http://dx.doi.org/10.1111/j.1469-7610.1996.tb01381.x] [PMID: 8655659]
[30]
Gaugler, T.; Klei, L.; Sanders, S.J.; Bodea, C.A.; Goldberg, A.P.; Lee, A.B.; Mahajan, M.; Manaa, D.; Pawitan, Y.; Reichert, J.; Ripke, S.; Sandin, S.; Sklar, P.; Svantesson, O.; Reichenberg, A.; Hultman, C.M.; Devlin, B.; Roeder, K.; Buxbaum, J.D. Most genetic risk for autism resides with common variation. Nat. Genet., 2014, 46(8), 881-885.
[http://dx.doi.org/10.1038/ng.3039] [PMID: 25038753]
[31]
Maurer, M.H. Genomic and proteomic advances in autism research. Electrophoresis, 2012, 33(24), 3653-3658.
[http://dx.doi.org/10.1002/elps.201200382] [PMID: 23160986]
[32]
Nolen, B.M.; Lokshin, A.E. Multianalyte assay systems in the differential diagnosis of ovarian cancer. Expert Opin. Med. Diagn., 2012, 6(2), 131-138.
[http://dx.doi.org/10.1517/17530059.2012.661711] [PMID: 22468148]
[33]
West, P.R.; Amaral, D.G.; Bais, P.; Smith, A.M.; Egnash, L.A.; Ross, M.E.; Palmer, J.A.; Fontaine, B.R.; Conard, K.R.; Corbett, B.A.; Cezar, G.G.; Donley, E.L.R.; Burrier, R.E. Metabolomics as a tool for discovery of biomarkers of autism spectrum disorder in the blood plasma of children. PLoS One, 2014, 9(11), e112445.
[http://dx.doi.org/10.1371/journal.pone.0112445] [PMID: 25380056]
[34]
Smith, A.M.; King, J.J.; West, P.R.; Ludwig, M.A.; Donley, E.L.R.; Burrier, R.E.; Amaral, D.G. Amino acid dysregulation metabotypes: Potential biomarkers for diagnosis and individualized treatment for subtypes of autism spectrum disorder. Biol. Psychiatry, 2019, 85(4), 345-354.
[http://dx.doi.org/10.1016/j.biopsych.2018.08.016] [PMID: 30446206]
[35]
Wang, H.; Liang, S.; Wang, M.; Gao, J.; Sun, C.; Wang, J.; Xia, W.; Wu, S.; Sumner, S.J.; Zhang, F.; Sun, C.; Wu, L. Potential serum biomarkers from a metabolomics study of autism. J. Psychiatry Neurosci., 2016, 41(1), 27-37.
[http://dx.doi.org/10.1503/jpn.140009] [PMID: 26395811]
[36]
Mota, F.S.B.; Nascimento, K.S.; Oliveira, M.V.; Osterne, V.J.S.; Clemente, J.C.M.; Correia-Neto, C.; Lima-Neto, A.B.; van Tilburg, M.F.; Leal-Cardoso, J.H.; Guedes, M.I.F.; Cavada, B.S. Potential protein markers in children with Autistic Spectrum Disorder (ASD) revealed by salivary proteomics. Int. J. Biol. Macromol., 2022, 199, 243-251.
[http://dx.doi.org/10.1016/j.ijbiomac.2022.01.011] [PMID: 35016969]
[37]
Abraham, J.; Szoko, N.; Natowicz, M.R. Proteomic investigations of autism spectrum disorder: Past findings, current challenges, and future prospects. Adv. Exp. Med. Biol., 2019, 1118, 235-252.
[http://dx.doi.org/10.1007/978-3-030-05542-4_12] [PMID: 30747426]
[38]
Vellingiri, B.; Aishwarya, S. Y.; Benita, J.S.; Sriram, A.G.; Winster, S.B.H.; Vijayakumar, P.; Narayanasamy, A.; Mariappan, S.; Sangeetha, R.; Valsala, G.A.; Parthasarathi, R.; Iyer, M. An anxious relationship between autism spectrum disorder and gut microbiota: A tangled chemistry? J. Clin. Neurosci., 2022, 99, 169- 189.
[http://dx.doi.org/10.1016/j.jocn.2022.03.003]
[39]
Yao, F.; Zhang, K.; Feng, C.; Gao, Y.; Shen, L.; Liu, X.; Ni, J. Protein biomarkers of autism spectrum disorder identified by computational and experimental methods. Front. Psychiatry, 2021, 12, 554621.
[http://dx.doi.org/10.3389/fpsyt.2021.554621] [PMID: 33716802]
[40]
Hewitson, L.; Mathews, J.A.; Devlin, M.; Schutte, C.; Lee, J.; German, D.C. Blood biomarker discovery for autism spectrum disorder: A proteomic analysis. PLoS One, 2021, 16(2), e0246581.
[http://dx.doi.org/10.1371/journal.pone.0246581] [PMID: 33626076]
[41]
Shen, L.; Liu, X.; Zhang, H.; Lin, J.; Feng, C.; Iqbal, J. Biomarkers in autism spectrum disorders: Current progress. Clin. Chim. Acta, 2020, 502, 41-54.
[http://dx.doi.org/10.1016/j.cca.2019.12.009] [PMID: 31857069]
[42]
Rigby, M.J.; Orefice, N.S.; Lawton, A.J.; Ma, M.; Shapiro, S.L.; Yi, S.Y.; Dieterich, I.A.; Frelka, A.; Miles, H.N.; Pearce, R.A.; Yu, J.P.J.; Li, L.; Denu, J.M.; Puglielli, L. Increased expression of SLC25A1/CIC causes an autistic-like phenotype with altered neuron morphology. Brain, 2022, 145(2), 500-516.
[http://dx.doi.org/10.1093/brain/awab295] [PMID: 35203088]
[43]
Nakamura, M.; Nakagami, A.; Nakagaki, K.; Yasue, M.; Kawai, N.; Ichinohe, N. Prenatal valproic acid-induced autism marmoset model exhibits higher salivary cortisol levels. Front. Behav. Neurosci., 2022, 16, 943759.
[http://dx.doi.org/10.3389/fnbeh.2022.943759] [PMID: 36035018]
[44]
Murtaza, N.; Uy, J.; Singh, K.K. Emerging proteomic approaches to identify the underlying pathophysiology of neurodevelopmental and neurodegenerative disorders. Mol. Autism, 2020, 11(1), 27.
[http://dx.doi.org/10.1186/s13229-020-00334-5] [PMID: 32317014]
[45]
Shen, L.; Zhang, K.; Feng, C.; Chen, Y.; Li, S.; Iqbal, J.; Liao, L.; Zhao, Y.; Zhai, J. iTRAQ-Based proteomic analysis reveals protein profile in plasma from children with autism. Proteomics Clin. Appl., 2018, 12(3), 1700085.
[http://dx.doi.org/10.1002/prca.201700085] [PMID: 29274201]
[46]
Abraham, J.R.; Szoko, N.; Barnard, J.; Rubin, R.A.; Schlatzer, D.; Lundberg, K.; Li, X.; Natowicz, M.R. Proteomic investigations of autism brain identify known and novel pathogenetic processes. Sci. Rep., 2019, 9(1), 13118.
[http://dx.doi.org/10.1038/s41598-019-49533-y] [PMID: 31511657]
[47]
Wei, H.; Ma, Y.; Liu, J.; Ding, C.; Hu, F.; Yu, L. Proteomic analysis of cortical brain tissue from the BTBR mouse model of autism: Evidence for changes in STOP and myelin-related proteins. Neuroscience, 2016, 312, 26-34.
[http://dx.doi.org/10.1016/j.neuroscience.2015.11.003] [PMID: 26562433]
[48]
Broek, J.A.C.; Guest, P.C.; Rahmoune, H.; Bahn, S. Proteomic analysis of post mortem brain tissue from autism patients: evidence for opposite changes in prefrontal cortex and cerebellum in synaptic connectivity-related proteins. Mol. Autism, 2014, 5(1), 41.
[http://dx.doi.org/10.1186/2040-2392-5-41] [PMID: 25126406]
[49]
Ilieva, M.; Aldana, B.I.; Vinten, K.T.; Hohmann, S.; Woofenden, T.W.; Lukjanska, R.; Waagepetersen, H.S.; Michel, T.M. Proteomic phenotype of cerebral organoids derived from autism spectrum disorder patients reveal disrupted energy metabolism, cellular components, and biological processes. Mol. Psychiatry, 2022, 27(9), 3749-3759.
[http://dx.doi.org/10.1038/s41380-022-01627-2] [PMID: 35618886]
[50]
Urresti, J.; Zhang, P.; Moran-Losada, P.; Yu, N.K.; Negraes, P.D.; Trujillo, C.A.; Antaki, D.; Amar, M.; Chau, K.; Pramod, A.B.; Diedrich, J.; Tejwani, L.; Romero, S.; Sebat, J.; Yates, J.R., III; Muotri, A.R.; Iakoucheva, L.M. Cortical organoids model early brain development disrupted by 16p11.2 copy number variants in autism. Mol. Psychiatry, 2021, 26(12), 7560-7580.
[http://dx.doi.org/10.1038/s41380-021-01243-6] [PMID: 34433918]
[51]
Wang, X.; Yang, Z.; Fang, S.; Zhang, Y.; Guo, J.; Gou, L. Declining levels of specialized synaptic surface proteins in nnos-expressing interneurons in mice treated prenatally with valproic acid. Neurochem. Res., 2021, 46(7), 1794-1800.
[http://dx.doi.org/10.1007/s11064-021-03326-w] [PMID: 33876374]
[52]
Mahony, C.; O’Ryan, C. Convergent canonical pathways in autism spectrum disorder from proteomic, transcriptomic and dna methylation data. Int. J. Mol. Sci., 2021, 22(19), 10757.
[http://dx.doi.org/10.3390/ijms221910757] [PMID: 34639097]
[53]
Taylor, L.E.; Swerdfeger, A.L.; Eslick, G.D. Vaccines are not associated with autism: An evidence-based meta-analysis of case-control and cohort studies. Vaccine, 2014, 32(29), 3623-3629.
[http://dx.doi.org/10.1016/j.vaccine.2014.04.085] [PMID: 24814559]
[54]
Bahmani, M.; Sarrafchi, A.; Shirzad, H.; Rafieian-Kopaei, M. Autism: Pathophysiology and promising herbal remedies. Curr. Pharm. Des., 2015, 22(3), 277-285.
[http://dx.doi.org/10.2174/1381612822666151112151529] [PMID: 26561063]
[55]
Shen, C.; Zhao, X.; Ju, W.; Zou, X.; Huo, L.; Yan, W.; Zou, J.; Yan, G.; Jenkins, E.C.; Brown, W.T.; Zhong, N. A proteomic investigation of B lymphocytes in an autistic family: a pilot study of exposure to natural rubber latex (NRL) may lead to autism. J. Mol. Neurosci., 2011, 43(3), 443-452.
[http://dx.doi.org/10.1007/s12031-010-9463-5] [PMID: 20957522]
[56]
Singh, S.; Yazdani, U.; Gadad, B.; Zaman, S.; Hynan, L.S.; Roatch, N.; Schutte, C.; Marti, C.N.; Hewitson, L.; German, D.C. Serum thyroid-stimulating hormone and interleukin-8 levels in boys with autism spectrum disorder. J. Neuroinflammation, 2017, 14(1), 113.
[http://dx.doi.org/10.1186/s12974-017-0888-4] [PMID: 28577577]
[57]
Ngounou Wetie, A.G.; Wormwood, K.L.; Russell, S.; Ryan, J.P.; Darie, C.C.; Woods, A.G. A pilot proteomic analysis of salivary biomarkers in autism spectrum disorder. Autism Res., 2015, 8(3), 338-350.
[http://dx.doi.org/10.1002/aur.1450] [PMID: 25626423]
[58]
Corbett, B.A.; Kantor, A.B.; Schulman, H.; Walker, W.L.; Lit, L.; Ashwood, P.; Rocke, D.M.; Sharp, F.R. A proteomic study of serum from children with autism showing differential expression of apolipoproteins and complement proteins. Mol. Psychiatry, 2007, 12(3), 292-306.
[http://dx.doi.org/10.1038/sj.mp.4001943] [PMID: 17189958]
[59]
Steeb, H.; Ramsey, J.M.; Guest, P.C.; Stocki, P.; Cooper, J.D.; Rahmoune, H.; Ingudomnukul, E.; Auyeung, B.; Ruta, L.; Baron-Cohen, S.; Bahn, S. Serum proteomic analysis identifies sex-specific differences in lipid metabolism and inflammation profiles in adults diagnosed with Asperger syndrome. Mol. Autism, 2014, 5(1), 4.
[http://dx.doi.org/10.1186/2040-2392-5-4] [PMID: 24467795]
[60]
Suganya, V.; Geetha, A. Urine proteome analysis to evaluate protein biomarkers in children with autism. Clin. Chim. Acta, 2015, 450, 210-219.
[http://dx.doi.org/10.1016/j.cca.2015.08.015] [PMID: 26296899]
[61]
Cortelazzo, A.; De Felice, C.; Guerranti, R.; Signorini, C.; Leoncini, S.; Zollo, G.; Leoncini, R.; Timperio, A.M.; Zolla, L.; Ciccoli, L. Expression and oxidative modifications of plasma proteins in autism spectrum disorders: Interplay between inflammatory response and lipid peroxidation. Proteomics Clin. Appl., 2016, 10(11), 1103-1112.
[http://dx.doi.org/10.1002/prca.201500076] [PMID: 27246309]
[62]
Kim, S.; Kim, H.; Yim, Y.S.; Ha, S.; Atarashi, K.; Tan, T.G.; Longman, R.S.; Honda, K.; Littman, D.R.; Choi, G.B.; Huh, J.R. Maternal gut bacteria promote neurodevelopmental abnormalities in mouse offspring. Nature, 2017, 549(7673), 528-532.
[http://dx.doi.org/10.1038/nature23910] [PMID: 28902840]
[63]
Desbonnet, L.; Clarke, G.; Shanahan, F.; Dinan, T.G.; Cryan, J.F. Microbiota is essential for social development in the mouse. Mol. Psychiatry, 2014, 19(2), 146-148.
[http://dx.doi.org/10.1038/mp.2013.65] [PMID: 23689536]
[64]
Jakobshagen, K.; Erny, D.; Staszewski, O.; Wieghofer, P.; Amit, I.; Chun, E.; Stecher, B.; Prinz, M.; Mahlakoi, V. Host microbiota constantly control maturation and function of microglia in the CNS. Nature Neurosci., 2013, 18, 965-977.
[http://dx.doi.org/10.1038/nn.4030]
[65]
McColl, E.R.; Piquette-Miller, M. Viral model of maternal immune activation alters placental AMPK and mTORC1 signaling in rats. Placenta, 2021, 112, 36-44.
[http://dx.doi.org/10.1016/j.placenta.2021.07.002] [PMID: 34256323]
[66]
Missault, S.; Van den Eynde, K.; Vanden Berghe, W.; Fransen, E.; Weeren, A.; Timmermans, J.P.; Kumar-Singh, S.; Dedeurwaerdere, S. The risk for behavioural deficits is determined by the maternal immune response to prenatal immune challenge in a neurodevelopmental model. Brain Behav. Immun., 2014, 42, 138-146.
[http://dx.doi.org/10.1016/j.bbi.2014.06.013] [PMID: 24973728]
[67]
Murray, K.N.; Edye, M.E.; Manca, M.; Vernon, A.C.; Oladipo, J.M.; Fasolino, V.; Harte, M.K.; Mason, V.; Grayson, B.; McHugh, P.C.; Knuesel, I.; Prinssen, E.P.; Hager, R.; Neill, J.C. Evolution of a maternal immune activation (mIA) model in rats: Early developmental effects. Brain Behav. Immun., 2019, 75, 48-59.
[http://dx.doi.org/10.1016/j.bbi.2018.09.005] [PMID: 30218784]
[68]
Györffy, B.A.; Gulyássy, P.; Gellén, B.; Völgyi, K.; Madarasi, D.; Kis, V.; Ozohanics, O.; Papp, I.; Kovács, P.; Lubec, G.; Dobolyi, Á.; Kardos, J.; Drahos, L.; Juhász, G.; Kékesi, K.A. Widespread alterations in the synaptic proteome of the adolescent cerebral cortex following prenatal immune activation in rats. Brain Behav. Immun., 2016, 56, 289-309.
[http://dx.doi.org/10.1016/j.bbi.2016.04.002] [PMID: 27058163]
[69]
Wang, Y.M.; Qiu, M.Y.; Liu, Q.; Tang, H.; Gu, H.F. Critical role of dysfunctional mitochondria and defective mitophagy in autism spectrum disorders. Brain Res. Bull., 2021, 168, 138-145.
[http://dx.doi.org/10.1016/j.brainresbull.2020.12.022] [PMID: 33400955]
[70]
Ngounou Wetie, A.G.; Wormwood, K.L.; Charette, L.; Ryan, J.P.; Woods, A.G.; Darie, C.C. Comparative two‐dimensional polyacrylamide gel electrophoresis of the salivary proteome of children with autism spectrum disorder. J. Cell. Mol. Med., 2015, 19(11), 2664-2678.
[http://dx.doi.org/10.1111/jcmm.12658] [PMID: 26290361]
[71]
Feng, C.; Chen, Y.; Pan, J.; Yang, A.; Niu, L.; Min, J.; Meng, X.; Liao, L.; Zhang, K.; Shen, L. Redox proteomic identification of carbonylated proteins in autism plasma: insight into oxidative stress and its related biomarkers in autism. Clin. Proteomics, 2017, 14(1), 2.
[http://dx.doi.org/10.1186/s12014-017-9138-0] [PMID: 28077936]
[72]
A, O.; U, M.; Lf, B.; A, G.C. Energy metabolism in childhood neurodevelopmental disorders. EBioMedicine, 2021, 69, 103474.
[http://dx.doi.org/10.1016/j.ebiom.2021.103474] [PMID: 34256347]
[73]
Zarate, Y.A.; Örsell, J.L.; Bosanko, K.; Srikanth, S.; Cascio, L.; Pauly, R.; Boccuto, L. Individuals with SATB2-associated syndrome with and without autism have a recognizable metabolic profile and distinctive cellular energy metabolism alterations. Metab. Brain Dis., 2021, 36(5), 1049-1056.
[http://dx.doi.org/10.1007/s11011-021-00706-7] [PMID: 33661512]
[74]
Kolar, D.; Kleteckova, L.; Brozka, H.; Vales, K. Mini-review: Brain energy metabolism and its role in animal models of depression, bipolar disorder, schizophrenia and autism. Neurosci. Lett., 2021, 760, 136003.
[http://dx.doi.org/10.1016/j.neulet.2021.136003] [PMID: 34098028]
[75]
Ngounou Wetie, A.G.; Wormwood, K.; Thome, J.; Dudley, E.; Taurines, R.; Gerlach, M.; Woods, A.G.; Darie, C.C. A pilot proteomic study of protein markers in autism spectrum disorder. Electrophoresis, 2014, 35(14), 2046-2054.
[http://dx.doi.org/10.1002/elps.201300370] [PMID: 24687421]
[76]
Akbari, M.; Kirkwood, T.B.L.; Bohr, V.A. Mitochondria in the signaling pathways that control longevity and health span. Ageing Res. Rev., 2019, 54, 100940.
[http://dx.doi.org/10.1016/j.arr.2019.100940] [PMID: 31415807]
[77]
Annesley, S.J.; Fisher, P.R. Mitochondria in health and disease. Cells, 2019, 8(7), 680.
[http://dx.doi.org/10.3390/cells8070680] [PMID: 31284394]
[78]
Nunnari, J.; Suomalainen, A. Mitochondria: In sickness and in health. Cell, 2012, 148(6), 1145-1159.
[http://dx.doi.org/10.1016/j.cell.2012.02.035] [PMID: 22424226]
[79]
Wong, S.; Giulivi, C. Autism, mitochondria and polybrominated diphenyl ether exposure. CNS Neurol. Disord. Drug Targets, 2016, 15(5), 614-623.
[http://dx.doi.org/10.2174/1871527315666160413122624] [PMID: 27071785]
[80]
Rossignol, D.A.; Frye, R.E. Mitochondrial dysfunction in autism spectrum disorders: A systematic review and meta-analysis. Mol. Psychiatry, 2012, 17(3), 290-314.
[http://dx.doi.org/10.1038/mp.2010.136] [PMID: 21263444]
[81]
Rojas-Charry, L.; Nardi, L.; Methner, A.; Schmeisser, M.J. Abnormalities of synaptic mitochondria in autism spectrum disorder and related neurodevelopmental disorders. J. Mol. Med., 2021, 99(2), 161-178.
[http://dx.doi.org/10.1007/s00109-020-02018-2] [PMID: 33340060]
[82]
Wang, Y.; Zhang, J.; Song, W.; Tian, X.; Liu, Y.; Wang, Y.; Ma, J.; Wang, C.; Yan, G. A proteomic analysis of urine biomarkers in autism spectrum disorder. J. Proteomics, 2021, 242, 104259.
[http://dx.doi.org/10.1016/j.jprot.2021.104259] [PMID: 33957315]
[83]
Xu, Z.; Zhang, X.; Chang, H.; Kong, Y.; Ni, Y.; Liu, R.; Zhang, X.; Hu, Y.; Yang, Z.; Hou, M.; Mao, R.; Liu, W.T.; Du, Y.; Yu, S.; Wang, Z.; Ji, M.; Zhou, Z. Rescue of maternal immune activation-induced behavioral abnormalities in adult mouse offspring by pathogen-activated maternal Treg cells. Nat. Neurosci., 2021, 24(6), 818-830.
[http://dx.doi.org/10.1038/s41593-021-00837-1] [PMID: 33859437]
[84]
McFarlane, H.G.; Kusek, G.K.; Yang, M.; Phoenix, J.L.; Bolivar, V.J.; Crawley, J.N. Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes Brain Behav., 2008, 7(2), 152-163.
[http://dx.doi.org/10.1111/j.1601-183X.2007.00330.x] [PMID: 17559418]
[85]
Stanton, J.E.; Malijauskaite, S.; McGourty, K.; Grabrucker, A.M. The metallome as a link between the “omes” in autism spectrum disorders. Front. Mol. Neurosci., 2021, 14, 695873.
[http://dx.doi.org/10.3389/fnmol.2021.695873] [PMID: 34290588]
[86]
Lakshmi Priya, M.D.; Geetha, A. A biochemical study on the level of proteins and their percentage of nitration in the hair and nail of autistic children. Clin. Chim. Acta, 2011, 412(11-12), 1036-1042.
[http://dx.doi.org/10.1016/j.cca.2011.02.021] [PMID: 21338594]
[87]
Hamoudi, W.; Tripathi, M.K.; Ojha, S.K.; Amal, H. A cross-talk between nitric oxide and the glutamatergic system in a Shank3 mouse model of autism. Free Radic. Biol. Med., 2022, 188, 83-91.
[http://dx.doi.org/10.1016/j.freeradbiomed.2022.06.007] [PMID: 35716826]
[88]
Bentea, E.; Villers, A.; Moore, C.; Funk, A.J.; O’Donovan, S.M.; Verbruggen, L.; Lara, O.; Janssen, P.; De Pauw, L.; Declerck, N.B.; DePasquale, E.A.K.; Churchill, M.J.; Sato, H.; Hermans, E.; Arckens, L.; Meshul, C.K.; Ris, L.; McCullumsmith, R.E.; Massie, A. Corticostriatal dysfunction and social interaction deficits in mice lacking the cystine/glutamate antiporter. Mol. Psychiatry, 2021, 26(9), 4754-4769.
[http://dx.doi.org/10.1038/s41380-020-0751-3] [PMID: 32366950]

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