Neurotrophin blood-based gene expression and social cognition analysis in patients with autism spectrum disorder

Neurogenetics

Volumn 16, Issue 2, 2015, Pages 123-131

  Segura, Mònica ^a   Pedreño, Carla ^b   Obiols, Jordi ^b   Taurines, Regina ^c   Pàmias, Montserrat ^d   Grünblatt, Edna ^e,f   Gella, Alejandro ^a,g,h  

^a UNIVERSITAT INTERNACIONAL DE CATALUNYA   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d Servicio de Oncología Médica   (Spain)

^e UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^f UNIVERSITY OF ZURICH   (Switzerland)

^g FEIL FAMILY BRAIN AND MIND RESEARCH INSTITUTE   (United States)

^h Sociedad Espanola de Bioquimica Clinica y Patologia Molecular   (Spain)

Author keywords

Advanced theory of mind; Autism spectrum disorder; Biomarkers; Endophenotypes; Gene expression; Neurotrophins

Indexed keywords

ANTIDEPRESSANT AGENT; MESSENGER RNA; NEUROLEPTIC AGENT; NEUROTROPHIN; NEUROTROPHIN RECEPTOR; BIOLOGICAL MARKER; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; BRAIN-DERIVED NEUROTROPHIC FACTOR, HUMAN; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR; NERVE PROTEIN; NEUROTROPHIN 3; NEUROTROPHIN 4; NGFR PROTEIN, HUMAN; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE A;

ADOLESCENT; ADULT; ALGORITHM; ARTICLE; AUTISM; AUTISM DIAGNOSTIC INTERVIEW REVISED; AUTISM DIAGNOSTIC OBSERVATION SCHEDULE; BDNF GENE; CLINICAL ARTICLE; CONTROLLED STUDY; DSM-IV; FEMALE; GENE; GENE EXPRESSION; HUMAN; IMAGINATION; INTELLIGENCE QUOTIENT; INTERPERSONAL COMMUNICATION; MALE; NT3 GENE; NT4 GENE; ONSET AGE; P75 NTR GENE; PRIORITY JOURNAL; QUANTITATIVE ASSAY; REAL TIME POLYMERASE CHAIN REACTION; SOCIAL COGNITION; SOCIAL INTERACTION; STEREOTYPY; THEORY OF MIND; TRKA GENE; TRKB GENE; BLOOD; CHILD; GENETICS; MIDDLE AGED; YOUNG ADULT;

ADOLESCENT; ADULT; AUTISM SPECTRUM DISORDER; BIOMARKERS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CHILD; FEMALE; GENE EXPRESSION; HUMANS; MALE; MIDDLE AGED; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEUROTROPHIN 3; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, TRKA; RECEPTOR, TRKB; RECEPTORS, NERVE GROWTH FACTOR; RNA, MESSENGER; THEORY OF MIND; YOUNG ADULT;

EID: 84925482130     PISSN: 13646745     EISSN: 13646753     Source Type: Journal    
DOI: 10.1007/s10048-014-0434-9     Document Type: Article

References (84)

1. Baird G, Simonoff E, Pickles A, Chandler S, Loucas T, Meldrum D et al (2006) Prevalence of disorders of the autism spectrum in a population cohort of children in South Thames: the Special Needs and Autism Project (SNAP). Lancet 368(9531):210–215
2. Howlin P, Goode S, Hutton J, Rutter M (2004) Adult outcome for children with autism. J Child Psychol Psychiatry 45(2):212–229
3. Zwaigenbaum L, Bryson S, Rogers T, Roberts W, Brian J, Szatmari P (2005) Behavioral manifestations of autism in the first year of life. Int J Dev Neurosci 23(2–3):143–152
4. Volkmar FR, Lord C, Bailey A, Schultz RT, Klin A (2004) Autism and pervasive developmental disorders. J Child Psychol Psychiatry 45(1):135–170
5. Pardo CA, Eberhart CG (2007) The neurobiology of autism. Brain Pathol 17(4):434–447
6. Belmonte MK, Allen G, Beckel-Mitchener A, Boulanger LM, Carper RA, Webb SJ (2004) Autism and abnormal development of brain connectivity. J Neurosci 24(42):9228–9231
7. Polleux F, Lauder JM (2004) Toward a developmental neurobiology of autism. Ment Retard Dev Disabil Res Rev 10(4):303–317
8. Folstein SE, Rosen-Sheidley B (2001) Genetics of autism: complex aetiology for a heterogeneous disorder. Nat Rev Genet 2(12):943–955
9. Freitag CM, Agelopoulos K, Huy E, Rothermundt M, Krakowitzky P, Meyer J, Deckert J, von Gontard A, Hohoff C (2010) Adenosine A(2A) receptor gene (ADORA2A) variants may increase autistic symptoms and anxiety in autism spectrum disorder. Eur Child Adolesc Psychiatry 19(1):67–74
10. Ruggeri B, Sarkans U, Schumann G, Persico AM (2014) Biomarkers in autism spectrum disorder: the old and the new. Psychopharmacology (Berl) 231(6):1201–1216
11. Glatt SJ, Tsuang MT, Winn M, Chandler SD, Collins M, Lopez L, Weinfeld M, Carter C, Schork N, Pierce K, Courchesne E (2012) Blood-based gene expression signatures of infants and toddlers with autism. J Am Acad Child Adolesc Psychiatry 51(9):934.e2–944.e2
12. Kong SW, Collins CD, Shimizu-Motohashi Y, Holm IA, Campbell MG, Lee IH, Brewster SJ, Hanson E, Harris HK, Lowe KR, Saada A, Mora A, Madison K, Hundley R, Egan J, McCarthy J, Eran A, Galdzicki M, Rappaport L, Kunkel LM, Kohane IS (2012) Characteristics and predictive value of blood transcriptome signature in males with autism spectrum disorders. PLoS One 7(12):e4947
13. Nickl-Jockschat T, Michel TM (2011) The role of neurotrophic factors in autism. Mol Psychiatry 16(5):478–490
14. Lang UE, Jockers-Scherübl MC, Hellweg R (2004) State of the art of the neurotrophin hypothesis in psychiatric disorders: implications and limitations. J Neural Transm 111(3):387–411
15. Leibrock J, Lottspeich F, Hohn A, Hofer M, Hengerer B, Masiakowski P et al (1989) Molecular cloning and expression of brain-derived neurotrophic factor. Nature 341(6238):149–152
16. Ernfors P, Ibanez CF, Ebendal T, Olson L, Persson H (1990) Molecular cloning and neurotrophic activities of a protein with structural similarities to nerve growth factor: developmental and topographical expression in the brain. Proc Natl Acad Sci 87(14):5454–5458
17. Klein R, Nanduri V, Jing S, Lamballe F, Tapley P, Bryant S et al (1991) The trkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3. Cell 66(2):395–403
18. Ip NY, Ibáñez CF, Nye SH, Mcclain J, Jones PF, Gies DR et al (1992) Mammalian neurotrophin-4: structure, chromosomal localization, tissue distribution, and receptor specificity. Proc Natl Acad Sci U S A 89(7):3060–3064
19. Klein R, Jing S, Nanduri V, O’Rourke E, Barbacid M (1991) The trk proto-oncogene encodes a receptor for nerve growth factor. Cell 65(1):189–197
20. Lamballe F, Klein R, Barbacid M (1991) trkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell 66(5):967–979
21. Soppet D, Escandon E, Maragos J, Middlemas DS, Reid SW, Blair J et al (1991) The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell 65(5):895–903
22. Squinto SP, Stitt TN, Aldrich TH, Davis S, Bianco SM, Radziejewski C et al (1991) trkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell 65(5):885–893
23. Hallböök F, Ibáñez CF, Persson H (1991) Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary. Neuron 6(5):845–858
24. Lee KF, Bachman K, Landis S, Jaenisch R (1994) Dependence on p75 for innervation of some sympathetic targets. Science 263(5152):1447–1449
25. Connolly AM, Chez M, Streif EM, Keeling RM, Golumbek PT, Kwon JM et al (2006) Brain-derived neurotrophic factor and autoantibodies to neural antigens in sera of children with autistic spectrum disorders, Landau-Kleffner syndrome, and epilepsy. Biol Psychiatry 59(4):354–363
26. Miyazaki K, Narita N, Sakuta R, Miyahara T, Naruse H, Okado N et al (2004) Serum neurotrophin concentrations in autism and mental retardation: a pilot study. Brain Dev 26(5):292–295
27. Nelson KB, Grether JK, Croen LA, Dambrosia JM, Dickens BF, Jelliffe LL et al (2001) Neuropeptides and neurotrophins in neonatal blood of children with autism or mental retardation. Ann Neurol 49(5):597–606
28. Perry EK (2001) Cholinergic activity in autism: abnormalities in the cerebral cortex and basal forebrain. Am J Psychiatry 158(7):1058–1066
29. Correia CT, Coutinho AM, Sequeira AF, Sousa IG, Lourenço Venda L, Almeida JP et al (2010) Increased BDNF levels and NTRK2 gene association suggest a disruption of BDNF/TrkB signaling in autism. Genes Brain Behav 9(7):841–848
30. Hashimoto K, Iwata Y, Nakamura K, Tsujii M, Tsuchiya KJ, Sekine Y et al (2006) Reduced serum levels of brain-derived neurotrophic factor in adult male patients with autism. Prog Neuropsychopharmacol Biol Psychiatry 30(8):1529–1531
31. Abdallah MW, Mortensen EL, Greaves-Lord K, Larsen N, Bonefeld-Jørgensen EC, Nørgaard-Pedersen B et al (2013) Neonatal levels of neurotrophic factors and risk of autism spectrum disorders. Acta Psychiatr Scand 128(1):61–69
32. Taurines R, Segura M, Schecklmann M, Albantakis L, Grünblatt E, Walitza S, Jans T, Lyttwin B, Haberhausen M, Theisen FM, Martin B, Briegel W, Thome J, Schwenck C, Romanos M, Gerlach M (2014) Altered peripheral BDNF mRNA expression and BDNF protein concentrations in blood of children and adolescents with autism spectrum disorder. J Neural Transm 121(9):1117–1128
33. Viding E, Blakemore SJ (2007) Endophenotype approach to developmental psychopathology: implications for autism research. Behav Genet 37(1):51–60
34. Baron-Cohen S (1991) The theory of mind deficit in autism: how specific is it? Br J Dev Psychol 9:301–314
35. Happé FG (1994) An advanced test of theory of mind: understanding of story characters’ thoughts and feelings by able autistic, mentally handicapped, and normal children and adults. J Autism Dev Disord 24(2):129–154
36. Dawson G, Carver L, Meltzoff AN, Panagiotides H, McPartland J, Webb SJ (2002) Neural correlates of face and object recognition in young children with autisms spectrum disorder, developmental delay, and typical development. Child Dev 73(3):700–717
37. Pierce K, Muller RA, Ambrose J, Allen G, Curchesne E (2001) Face processing occurs outside the fusiform “face area” in autism: evidence from function MRI. Brain 124(Pt 10):2059–2073
38. Karege F, Schwald M, Cisse M (2002) Postnatal developmental profile of brain-derived neurotrophic factor in rat brain and platelets. Neurosci Lett 328(3):261–264
39. Katoh-Semba R, Wakako R, Komori T, Shigemi H, Miyazaki N, Ito H, Kumagai T, Tsuzuki M, Shigemi K, Yoshida F, Nakayama A (2007) Age-related changes in BDNF protein levels in human serum: differences between autism cases and normal controls. Int J Dev Neurosci 25(6):367–372
40. Lord C, Rutter M, Couteur A (1994) Autism diagnostic interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord 24(5):659–685
41. Lord C, Risi S, Lambrecht L, Cook EH, Leventhal BL, Dilavore PC et al (2000) The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord 30(3):205–223
42. Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I (2001) The “Reading the Mind in the Eyes” test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. J Child Psychol Psychiatry 42(2):241–251
43. Baron-Cohen S, Ring HA, Wheelwright S, Bullmore ET, Brammer MJ, Simmons A et al (1999) Social intelligence in the normal and autistic brain: an fMRI study. Eur J Neurosci 11(6):1891–1898
44. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A et al (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(7), RESEARCH0034
45. Tostes MH, Teixeira HC, Gattaz WF, Brandão MA, Raposo NR (2012) Altered neurotrophin, neuropeptide, cytokines and nitric oxide levels in autism. Pharmacopsychiatry 45(6):241–243
46. Sajdel-Sulkowska EM, Xu M, McGinnis W, Koibuchi N (2011) Brain region-specific changes in oxidative stress and neurotrophin levels in autism spectrum disorders (ASD). Cerebellum 10(1):43–48
47. Xu M, Sajdel-Sulkowska EM, Iwasaki T, Koibuchi N (2013) Aberrant cerebellar neurotrophin-3 expression induced by lipopolysaccharide exposure during brain development. Cerebellum 12(3):316–318
48. Sherrard RM, Bower AJ (2002) Climbing fiber development: do neurotrophins have a part to play? Cerebellum 1(4):265–275
49. Whitney ER, Kemper TL, Rosene DL, Bauman ML, Blatt GJ (2009) Density of cerebellar basket and stellate cells in autism: evidence for a late developmental loss of Purkinje cells. J Neurosci Res 87(10):2245–2254
50. Ritvo ER, Freeman BJ, Scheibel AB, Duong T, Robinson H, Guthrie D, Ritvo A (1986) Lower Purkinje cell counts in the cerebella of four autistic subjects: initial findings of the UCLA-NSAC Autopsy Research Report. Am J Psychiatry 143(7):862–866
51. Mount HT, Dreyfus CF, Black IB (1994) Neurotrophin-3 selectively increases cultured Purkinje cell survival. Neuroreport 5(18):2497–2500
52. Sudarov A (2013) Defining the role of cerebellar Purkinje cells in autism spectrum disorders. Cerebellum 12(6):950–955
53. Bauman ML, Kemper TL (2005) Neuroanatomic observations of the brain in autism: a review and future directions. Int J Dev Neurosci 23(2–3):183–187
54. Coulson EJ (1999) p75 neurotrophin receptor-mediated neuronal death is promoted by Bcl-2 and prevented by Bcl-xL. J Biol Chem [Internet] 274(23):16387–16391
55. Frade JM, Rodríguez-Tébar A, Barde YA (1996) Induction of cell death by endogenous nerve growth factor through its p75 receptor. Nature 383(6596):166–168
56. Friedman WJ, Greene LA (1999) Neurotrophin signaling via Trks and p75. Exp Cell Res 253(1):131–142
57. Lee R, Kermani P, Teng KK, Hempstead BL (2001) Regulation of cell survival by secreted proneurotrophins. Science 294(5548):1945–1948
58. Volosin M, Song W, Almeida RD, Kaplan DR, Hempstead BL, Friedman WJ (2006) Interaction of survival and death signaling in basal forebrain neurons: roles of neurotrophins and proneurotrophins. J Neurosci 26(29):7756–7766
59. De Graaf-Peters VB, Hadders-Algra M (2006) Ontogeny of the human central nervous system: what is happening when? Early Hum Dev 82(4):257–266
60. Wei H, Alberts I, Li X (2014) The apoptotic perspective of autism. Int J Dev Neurosci 36:13–18
61. Sheikh AM, Malik M, Wen G, Chauhan A, Chauhan V, Gong CX, Liu F, Brown WT, Li X (2010) BDNF-Akt-Bcl2 antiapoptotic signaling pathway is compromised in the brain of autistic subjects. J Neurosci Res 88(12):2641–2647
62. Siniscalco D, Sapone A, Giordano C, Cirillo A, de Novellis V, de Magistris L, Rossi F, Fasano A, Maione S, Antonucci N (2012) The expression of caspases is enhanced in peripheral blood mononuclear cells of autism spectrum disorder patients. J Autism Dev Disord 42(7):1403–1410
63. Malik M, Sheikh AM, Wen G, Spivack W, Brown WT, Li X (2011) Expression of inflammatory cytokines, Bcl2 and cathepsin D are altered in lymphoblasts of autistic subjects. Immunobiology 216(1–2):80–85
64. Benedetti M, Levi A, Chao MV (1993) Differential expression of nerve growth factor receptors leads to altered binding affinity and neurotrophin responsiveness. Proc Natl Acad Sci U S A 90(16):7859–7863
65. Verdi JM, Birren SJ, Ibáñez CF, Persson H, Kaplan DR, Benedetti M, Chao MV, Anderson DJ (1994) p75LNGFR regulates Trk signal transduction and NGF-induced neuronal differentiation in MAH cells. Neuron 12(4):733–745
66. Gottesman II, Gould TD (2003) The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry 160:636–645
67. Warrier V, Baron-Cohen S, Chakrabarti B (2013) Genetic variation in GABRB3 is associated with Asperger syndrome and multiple endophenotypes relevant to autism. Mol Autism 4(1):48
68. Baron-Cohen S, O’Riordan M, Stone V, Jones R, Plaisted K (1999) Recognition of faux pas by normally developing children and children with Asperger syndrome or high-functioning autism. J Autism Dev Disord 29(5):407–418
69. Kaland N, Moller-Nielsen A, Callesen K, Mortensen EL, Gottlieb D, Smith L (2002) A new ‘advanced’ test of theory of mind: evidence from children and adolescents with Asperger syndrome. J Child Psychol Psychiatry 43(4):517–528
70. Spek AA, Scholte EM, Van Berckelaer-Onnes IA (2010) Theory of mind in adults with HFA and Asperger syndrome. J Autism Dev Disord 40(3):280–289
71. Zalla T, Sav AM, Stopin A, Ahade S, Leboyer M (2009) Faux pas detection and intentional action in Asperger Syndrome. A replication on a french sample. J Autism Dev Disord 39(2):373–382
72. Tager-Flusberg H, Sullivan K (2000) A componential view of theory of mind: evidence from Williams syndrome. Cognition 76(1):59–90
73. Ponnet KS, Roeyers H, Buysse A, De Clercq A, Van der Heyden E (2004) Advanced mind-reading in adults with Asperger syndrome. Autism 8(3):249–266
74. Kaland N, Callesen K, Møller-Nielsen A, Mortensen EL, Smith L (2008) Performance of children and adolescents with Asperger syndrome or high-functioning autism on advanced theory of mind tasks. J Autism Dev Disord 38(6):1112–1123
75. Scaccianoce S, Del Bianco P, Paolone G, Caprioli D, Modafferi AM, Nencini P, Badiani A (2006) Social isolation selectively reduces hippocampal brain-derived neurotrophic factor without altering plasma corticosterone. Behav Brain Res 168(2):323–325
76. Hashimoto K, Shimizu E, Iyo M (2004) Critical role of brain-derived neurotrophic factor in mood disorders. Brain Res Brain Res Rev 45(2):104–114, Review
77. Buitelaar JK, van der Wees M, Swaab-Barneveld H, van der Gaag RJ (1999) Theory of mind and emotion-recognition functioning in autistic spectrum disorders and in psychiatric control and normal children. Dev Psychopathol 11(1):39–58
78. Geurts HM, Verté S, Oosterlaan J, Roeyers H, Hartman CA, Mulder EJ, Berckelaer-Onnes IA, Sergeant JA (2004) Can the children’s communication checklist differentiate between children with autism, children with ADHD, and normal controls? J Child Psychol Psychiatry 45(8):1437–1453
79. Sergeant JA, Geurts H, Oosterlaan J (2002) How specific is a deficit of executive functioning for attention-deficit/hyperactivity disorder? Behav Brain Res 130(1–2):3–28, Review
80. Dorris L, Espie CA, Knott F, Salt J (2004) Mind-reading difficulties in the siblings of people with Asperger’s syndrome: evidence for a genetic influence in the abnormal development of a specific cognitive domain. J Child Psychol Psychiatry 45(2):412–418
81. Castelli F, Frith C, Happé F, Frith U (2002) Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. Brain 125(Pt 8):1839–1849
82. Sullivan PF, Fan C, Perou CM (2006) Evaluating the comparability of gene expression in blood and brain. Am J Med Genet B Neuropsychiatr Genet 141B(3):261–268
83. Rollins B, Martin MV, Morgan L, Vawter MP (2010) Analysis of whole genome biomarker expression in blood and brain. Am J Med Genet B Neuropsychiatr Genet 153B(4):919–936
84. Hayashi-Takagi A, Vawter MP, Iwamoto K (2014) Peripheral biomarkers revisited: integrative profiling of peripheral samples for psychiatric research. Biol Psychiatry 75(12):920–928