The apoptotic perspective of autism

International Journal of Developmental Neuroscience

Volumn 36, Issue , 2014, Pages 13-18

  Wei, Hongen ^a   Alberts, Ian ^b   Li, Xiaohong ^c  

^a SHANXI MEDICAL UNIVERSITY   (China)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

Author keywords

Apoptosis; Autism; Mechanism; Protein; Signaling pathway

Indexed keywords

4 AMINOBUTYRIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; CASPASE; CASPASE 3; CATHEPSIN D; GLUTAMIC ACID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN P53; RAF PROTEIN; RAS PROTEIN;

APOPTOSIS; ARTICLE; AUTISM; BRAIN DEVELOPMENT; BRAIN MATURATION; BRAIN SIZE; CEREBELLUM; DEGENERATIVE DISEASE; EXCITOTOXICITY; HUMAN; LYMPHOBLAST; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; COMPLICATION; DEVELOPMENTAL DISABILITIES; PATHOLOGY; PHYSIOLOGY;

ANIMALS; APOPTOSIS; AUTISTIC DISORDER; DEVELOPMENTAL DISABILITIES; HUMANS; OXIDATIVE STRESS;

EID: 84901347920     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2014.04.004     Document Type: Article

References (91)

1. Amaral D.G., Schumann C.M., Nordahl C.W. Neuroanatomy of autism. Trends Neurosci. 2008, 31:137-145.
2. Andermarcher E., Surani M.A., Gherardi E. Co-expression of the HGF/SF and c-met genes during early mouse embryogenesis precedes reciprocal expression in adjacent tissues during organogenesis. Dev. Genet. 1996, 18:254-266.
3. Angelidou A., Francis K., Vasiadi M., Alysandratos K.D., Zhang B., Theoharides A., Lykouras L., Sideri K., Kalogeromitros D., Theoharides T.C. Neurotensin is increased in serum of young children with autistic disorder. J. Neuroinflamm. 2010, 7:48.
4. Araghi-Niknam M., Fatemi S.H. Levels of Bcl-2 and P53 are altered in superior frontal and cerebellar cortices of autistic subjects. Cell. Mol. Neurobiol. 2003, 23:945-952.
5. Baron C.A., Tepper C.G., Liu S.Y., Davis R.R., Wang N.J., Schanen N.C., Gregg J.P. Genomic and functional profiling of duplicated chromosome 15 cell lines reveal regulatory alterations in UBE3A-associated ubiquitin-proteasome pathway processes. Hum. Mol. Genet. 2006, 15:853-869.
6. Bauman M., Kemper T.L. Histoanatomic observations of the brain in early infantile autism. Neurology 1985, 35:866-874.
7. Bauman M.L., Kemper T.L. Neuroanatomic observations of the brain in autism: a review and future directions. Int. J. Dev. Neurosci. 2005, 23:183-187.
8. Bibel M., Barde Y.A. Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev. 2000, 14:2919-2937.
9. Buttarelli F.R., Circella A., Pellicano C., Pontieri F.E. Dopamine transporter immunoreactivity in peripheral blood mononuclear cells in amyotrophic lateral sclerosis. Eur. J. Neurol. 2006, 13:416-418.
10. Buttke T.M., Sandstrom P.A. Oxidative stress as a mediator of apoptosis. Immunol. Today 1994, 15:7-10.
11. Campbell D.B., D'Oronzio R., Garbett K., Ebert P.J., Mirnics K., Levitt P., Persico A.M. Disruption of cerebral cortex MET signaling in autism spectrum disorder. Ann. Neurol. 2007, 62:243-250.
12. Cavanaugh J.E. Role of extracellular signal regulated kinase 5 in neuronal survival. Eur. J. Biochem. 2004, 271:2056-2059.
13. Chen J., Alberts I., Li X. Dysregulation of the IGF-I/PI3K/AKT/mTOR signaling pathway in autism spectrum disorders. Int. J. Dev. Neurosci. 2014, 35C:35-41.
14. Cheng Y., Corbin J.G., Levy R.J. Programmed cell death is impaired in the developing brain of FMR1 mutants. Dev. Neurosci. 2013, 35:347-358.
15. Courchesne E., Campbell K., Solso S. Brain growth across the life span in autism: age-specific changes in anatomical pathology. Brain Res. 2011, 1380:138-145.
16. Courchesne E., Mouton P.R., Calhoun M.E., Semendeferi K., Ahrens-Barbeau C., Hallet M.J., Barnes C.C., Pierce K. Neuron number and size in prefrontal cortex of children with autism. JAMA 2011, 306:2001-2010.
17. Culmsee C., Mattson M.P. p53 in neuronal apoptosis. Biochem. Biophys. Res. Commun. 2005, 331:761-777.
18. Davis S., Laroche S. Mitogen-activated protein kinase/extracellular regulated kinase signalling and memory stabilization: a review. Genes Brain Behav. 2006, 5(Suppl. 2):61-72.
19. Deiss L.P., Galinka H., Berissi H., Cohen O., Kimchi A. Cathepsin D protease mediates programmed cell death induced by interferon-gamma, Fas/APO-1 and TNF-alpha. EMBO J. 1996, 15:3861-3870.
20. Egaas B., Courchesne E., Saitoh O. Reduced size of corpus callosum in autism. Arch. Neurol. 1995, 52:794-801.
21. El-Ansary A.K., Bacha A.B., Kotb M. Etiology of autistic features: the persisting neurotoxic effects of propionic acid. J. Neuroinflamm. 2012, 9:74.
22. El-Ansary A.K., Ben Bacha A.G., Al-Ayadhi L.Y. Proinflammatory and proapoptotic markers in relation to mono and di-cations in plasma of autistic patients from Saudi Arabia. J. Neuroinflamm. 2011, 8:142.
23. Erdmann S., Ricken A., Hummitzsch K., Merkwitz C., Schliebe N., Gaunitz F., Strotmann R., Spanel-Borowski K. Inflammatory cytokines increase extracellular procathepsin D in permanent and primary endothelial cell cultures. Eur. J. Cell Biol. 2008, 87:311-323.
24. Fatemi S.H., Halt A.R. Altered levels of Bcl2 and p53 proteins in parietal cortex reflect deranged apoptotic regulation in autism. Synapse 2001, 42:281-284.
25. Fatemi S.H., Halt A.R., Stary J.M., Realmuto G.M., Jalali-Mousavi M. Reduction in anti-apoptotic protein Bcl-2 in autistic cerebellum. Neuroreport 2001, 12:929-933.
26. Fatemi S.H., Reutiman T.J., Folsom T.D., Thuras P.D. GABA(A) receptor downregulation in brains of subjects with autism. J. Autism Dev. Disord. 2009, 39:223-230.
27. Fatemi S.H., Stary J.M., Halt A.R., Realmuto G.R. Dysregulation of Reelin and Bcl-2 proteins in autistic cerebellum. J. Autism Dev. Disord. 2001, 31:529-535.
28. Franke T.F., Hornik C.P., Segev L., Shostak G.A., Sugimoto C. PI3K/Akt and apoptosis: size matters. Oncogene 2003, 22:8983-8998.
29. Frebel K., Wiese S. Signalling molecules essential for neuronal survival and differentiation. Biochem. Soc. Trans. 2006, 34:1287-1290.
30. Fusek M., Vetvickova J., Vetvicka V. Secretion of cytokines in breast cancer cells: the molecular mechanism of procathepsin D proliferative effects. J. Interferon Cytokine Res. 2007, 27:191-199.
31. Gatto C.L., Broadie K. Fragile X mental retardation protein is required for programmed cell death and clearance of developmentally-transient peptidergic neurons. Dev. Biol. 2011, 356:291-307.
32. Ghanizadeh A. Targeting neurotensin as a potential novel approach for the treatment of autism. J. Neuroinflamm. 2010, 7:58.
33. Grunnet L.G., Aikin R., Tonnesen M.F., Paraskevas S., Blaabjerg L., Storling J., Rosenberg L., Billestrup N., Maysinger D., Mandrup-Poulsen T. Proinflammatory cytokines activate the intrinsic apoptotic pathway in beta-cells. Diabetes 2009, 58:1807-1815.
34. Harada M., Taki M.M., Nose A., Kubo H., Mori K., Nishitani H., Matsuda T. Non-invasive evaluation of the GABAergic/glutamatergic system in autistic patients observed by MEGA-editing proton MR spectroscopy using a clinical 3tesla instrument. J. Autism Dev. Disord. 2011, 41:447-454.
35. Hartmann A., Hunot S., Michel P.P., Muriel M.P., Vyas S., Faucheux B.A., Mouatt-Prigent A., Turmel H., Srinivasan A., Ruberg M., Evan G.I., Agid Y., Hirsch E.C. Caspase-3: a vulnerability factor and final effector in apoptotic death of dopaminergic neurons in Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:2875-2880.
36. Hong S.E., Shugart Y.Y., Huang D.T., Shahwan S.A., Grant P.E., Hourihane J.O., Martin N.D., Walsh C.A. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat. Genet. 2000, 26:93-96.
37. Huang E.J., Reichardt L.F. Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 2003, 72:609-642.
38. Jarskog L.F., Gilmore J.H., Selinger E.S., Lieberman J.A. Cortical bcl-2 protein expression and apoptotic regulation in schizophrenia. Biol. Psychiatry 2000, 48:641-650.
39. Jarskog L.F., Glantz L.A., Gilmore J.H., Lieberman J.A. Apoptotic mechanisms in the pathophysiology of schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29:846-858.
40. Jarskog L.F., Selinger E.S., Lieberman J.A., Gilmore J.H. Apoptotic proteins in the temporal cortex in schizophrenia: high Bax/Bcl-2 ratio without caspase-3 activation. Am. J. Psychiatry 2004, 161:109-115.
41. Jung W., Castren E., Odenthal M., Vande Woude G.F., Ishii T., Dienes H.P., Lindholm D., Schirmacher P. Expression and functional interaction of hepatocyte growth factor-scatter factor and its receptor c-met in mammalian brain. J. Cell Biol. 1994, 126:485-494.
42. Katoh-Semba R., Wakako R., Komori T., Shigemi H., Miyazaki N., Ito H., Kumagai T., Tsuzuki M., Shigemi K., Yoshida F., Nakayama A. Age-related changes in BDNF protein levels in human serum: differences between autism cases and normal controls. Int. J. Dev. Neurosci. 2007, 25:367-372.
43. Kemper T.L., Bauman M.L. Neuropathology of infantile autism. Mol. Psychiatry 2002, 7(Suppl. 2):S12-S13.
44. Kyrylenko S., Roschier M., Korhonen P., Salminen A. Regulation of PTEN expression in neuronal apoptosis. Brain Res. Mol. Brain Res. 1999, 73:198-202.
45. Levitt P., Campbell D.B. The genetic and neurobiologic compass points toward common signaling dysfunctions in autism spectrum disorders. J. Clin. Invest. 2009, 119:747-754.
46. Li X., Chauhan A., Sheikh A.M., Patil S., Chauhan V., Li X.M., Ji L., Brown T., Malik M. Elevated immune response in the brain of autistic patients. J. Neuroimmunol. 2009, 207:111-116.
47. Loh K.P., Huang S.H., De Silva R., Tan B.K., Zhu Y.Z. Oxidative stress: apoptosis in neuronal injury. Curr. Alzheimer Res. 2006, 3:327-337.
48. MacFabe D.F., Rodríguez-Capote K., Franklin J.E., Kavaliers M., Possmayer F., Ossenkopp K.-P., Franklin A.E. A novel rodent model of autism: intraventricular infusions of propionic acid increase locomotor activity and induce neuroinflammation and oxidative stress in discrete regions of adult rat brain. Am. J. Biochem. Biotechnol. 2008, 4:146-166.
49. Mahadik S.P., Evans D., Lal H. Oxidative stress and role of antioxidant and omega-3 essential fatty acid supplementation in schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 2001, 25:463-493.
50. Maina F., Hilton M.C., Ponzetto C., Davies A.M., Klein R. Met receptor signaling is required for sensory nerve development and HGF promotes axonal growth and survival of sensory neurons. Genes Dev. 1997, 11:3341-3350.
51. Malik M., Sheikh A.M., Wen G., Spivack W., Brown W.T., Li X. Expression of inflammatory cytokines, Bcl2 and cathepsin D are altered in lymphoblasts of autistic subjects. Immunobiology 2011, 216:80-85.
52. Margolis R.L., Chuang D.M., Post R.M. Programmed cell death: implications for neuropsychiatric disorders. Biol. Psychiatry 1994, 35:946-956.
53. Masliah E., Mallory M., Alford M., Tanaka S., Hansen L.A. Caspase dependent DNA fragmentation might be associated with excitotoxicity in Alzheimer disease. J. Neuropathol. Exp. Neurol. 1998, 57:1041-1052.
54. Miyazaki K., Narita N., Sakuta R., Miyahara T., Naruse H., Okado N., Narita M. Serum neurotrophin concentrations in autism and mental retardation: a pilot study. Brain Dev. 2004, 26:292-295.
55. Murphy L.O., Blenis J. MAPK signal specificity: the right place at the right time. Trends Biochem. Sci. 2006, 31:268-275.
56. Nazeer A., Ghaziuddin M. Autism spectrum disorders: clinical features and diagnosis. Pediatr. Clin. N. Am. 2012, 59:19-25.
57. Nelson K.B., Grether J.K., Croen L.A., Dambrosia J.M., Dickens B.F., Jelliffe L.L., Hansen R.L., Phillips T.M. Neuropeptides and neurotrophins in neonatal blood of children with autism or mental retardation. Ann. Neurol. 2001, 49:597-606.
58. Olczak M., Duszczyk M., Mierzejewski P., Wierzba-Bobrowicz T., Majewska M.D. Lasting neuropathological changes in rat brain after intermittent neonatal administration of thimerosal. Folia Neuropathol. 2010, 48:258-269.
59. Organ S.L., Tsao M.S. An overview of the c-MET signaling pathway. Ther. Adv. Med. Oncol. 2011, 3:S7-S19.
60. Pardo C.A., Eberhart C.G. The neurobiology of autism. Brain Pathol. 2007, 17:434-447.
61. Piven J., Bailey J., Ranson B.J., Arndt S. An MRI study of the corpus callosum in autism. Am. J. Psychiatry 1997, 154:1051-1056.
62. Ritvo E.R., Freeman B.J., Scheibel A.B., Duong T., Robinson H., Guthrie D., Ritvo A. Lower Purkinje cell counts in the cerebella of four autistic subjects: initial findings of the UCLA-NSAC Autopsy Research Report. Am. J. Psychiatry 1986, 143:862-866.
63. Rudie J.D., Hernandez L.M., Brown J.A., Beck-Pancer D., Colich N.L., Gorrindo P., Thompson P.M., Geschwind D.H., Bookheimer S.Y., Levitt P., Dapretto M. Autism-associated promoter variant in MET impacts functional and structural brain networks. Neuron 2012, 75:904-915.
64. Sasaki T., Kitagawa K., Yagita Y., Sugiura S., Omura-Matsuoka E., Tanaka S., Matsushita K., Okano H., Tsujimoto Y., Hori M. Bcl2 enhances survival of newborn neurons in the normal and ischemic hippocampus. J. Neurosci. Res. 2006, 84:1187-1196.
65. Schumann C.M., Hamstra J., Goodlin-Jones B.L., Lotspeich L.J., Kwon H., Buonocore M.H., Lammers C.R., Reiss A.L., Amaral D.G. The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J. Neurosci. 2004, 24:6392-6401.
66. Sheikh A.M., Li X., Wen G., Tauqeer Z., Brown W.T., Malik M. Cathepsin D and apoptosis related proteins are elevated in the brain of autistic subjects. Neuroscience 2010, 165:363-370.
67. Sheikh A.M., Malik M., Wen G., Chauhan A., Chauhan V., Gong C.X., Liu F., Brown W.T., Li X. BDNF-Akt-Bcl2 antiapoptotic signaling pathway is compromised in the brain of autistic subjects. J. Neurosci. Res. 2010, 88:2641-2647.
68. Shen Y., White E. p53-dependent apoptosis pathways. Adv. Cancer Res. 2001, 82:55-84.
69. Shinohe A., Hashimoto K., Nakamura K., Tsujii M., Iwata Y., Tsuchiya K.J., Sekine Y., Suda S., Suzuki K., Sugihara G., Matsuzaki H., Minabe Y., Sugiyama T., Kawai M., Iyo M., Takei N., Mori N. Increased serum levels of glutamate in adult patients with autism. Prog. Neuropsychopharmacol. Biol. Psychiatry 2006, 30:1472-1477.
70. Silver W.G., Rapin I. Neurobiological basis of autism. Pediatr. Clin. N. Am. 2012, 59:45-61.
71. Siniscalco D., Sapone A., Giordano C., Cirillo A., de Novellis V., de Magistris L., Rossi F., Fasano A., Maione S., Antonucci N. The expression of caspases is enhanced in peripheral blood mononuclear cells of autism spectrum disorder patients. J. Autism Dev. Disord. 2012, 42:1403-1410.
72. Song M.S., Salmena L., Pandolfi P.P. The functions and regulation of the PTEN tumour suppressor. Nat. Rev. Mol. Cell Biol. 2012, 13:283-296.
73. Sonnenberg E., Meyer D., Weidner K.M., Birchmeier C. Scatter factor/hepatocyte growth factor and its receptor, the c-met tyrosine kinase, can mediate a signal exchange between mesenchyme and epithelia during mouse development. J. Cell Biol. 1993, 123:223-235.
74. Sparks B.F., Friedman S.D., Shaw D.W., Aylward E.H., Echelard D., Artru A.A., Maravilla K.R., Giedd J.N., Munson J., Dawson G., Dager S.R. Brain structural abnormalities in young children with autism spectrum disorder. Neurology 2002, 59:184-192.
75. Stigler K.A., McDonald B.C., Anand A., Saykin A.J., McDougle C.J. Structural and functional magnetic resonance imaging of autism spectrum disorders. Brain Res. 2011, 1380:146-161.
76. Takeuchi K., Gertner M.J., Zhou J., Parada L.F., Bennett M.V., Zukin R.S. Dysregulation of synaptic plasticity precedes appearance of morphological defects in a Pten conditional knockout mouse model of autism. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:4738-4743.
77. Trusolino L., Bertotti A., Comoglio P.M. MET signalling: principles and functions in development, organ regeneration and cancer. Nat. Rev. Mol. Cell Biol. 2010, 11:834-848.
78. Tulasne D., Deheuninck J., Lourenco F.C., Lamballe F., Ji Z., Leroy C., Puchois E., Moumen A., Maina F., Mehlen P., Fafeur V. Proapoptotic function of the MET tyrosine kinase receptor through caspase cleavage. Mol. Cell Biol. 2004, 24:10328-10339.
79. Uddin L.Q., Menon V., Young C.B., Ryali S., Chen T., Khouzam A., Minshew N.J., Hardan A.Y. Multivariate searchlight classification of structural magnetic resonance imaging in children and adolescents with autism. Biol. Psychiatry 2011, 70:833-841.
80. Vargas D.L., Nascimbene C., Krishnan C., Zimmerman A.W., Pardo C.A. Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann. Neurol. 2005, 57:67-81.
81. Wei H., Malik M., Sheikh A.M., Merz G., Ted Brown W., Li X. Abnormal cell properties and down-regulated FAK-Src complex signaling in B lymphoblasts of autistic subjects. Am. J. Pathol. 2011, 179:66-74.
82. Weiss L.A., Shen Y., Korn J.M., Arking D.E., Miller D.T., Fossdal R., Saemundsen E., Stefansson H., Ferreira M.A., Green T., Platt O.S., Ruderfer D.M., Walsh C.A., Altshuler D., Chakravarti A., Tanzi R.E., Stefansson K., Santangelo S.L., Gusella J.F., Sklar P., Wu B.L., Daly M.J. Association between microdeletion and microduplication at 16p11.2 and autism. N. Engl. J. Med. 2008, 358:667-675.
83. Wright K., Kolios G., Westwick J., Ward S.G. Cytokine-induced apoptosis in epithelial HT-29 cells is independent of nitric oxide formation. Evidence for an interleukin-13-driven phosphatidylinositol 3-kinase-dependent survival mechanism. J. Biol. Chem. 1999, 274:17193-17201.
84. Xiao G.H., Jeffers M., Bellacosa A., Mitsuuchi Y., Vande Woude G.F., Testa J.R. Anti-apoptotic signaling by hepatocyte growth factor/Met via the phosphatidylinositol 3-kinase/Akt and mitogen-activated protein kinase pathways. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:247-252.
85. Yang K., Cao F., Sheikh A.M., Malik M., Wen G., Wei H., Ted Brown W., Li X. Up-regulation of Ras/Raf/ERK1/2 signaling impairs cultured neuronal cell migration, neurogenesis, synapse formation, and dendritic spine development. Brain Struct. Funct. 2013, 218:669-682.
86. Yin A., Qiu Y., Jia B., Song T., Yu Y., Alberts I., Zhong M. The developmental pattern of the RAS/RAF/Erk1/2 pathway in the BTBR autism mouse model. Int. J. Dev. Neurosci. 2014, 10.1016/j.ijdevneu.2014.01.006.
87. Yochum C.L., Dowling P., Reuhl K.R., Wagner G.C., Ming X. VPA-induced apoptosis and behavioral deficits in neonatal mice. Brain Res. 2008, 1203:126-132.
88. Zhang Y., Bhavnani B.R. Glutamate-induced apoptosis in neuronal cells is mediated via caspase-dependent and independent mechanisms involving calpain and caspase-3 proteases as well as apoptosis inducing factor (AIF) and this process is inhibited by equine estrogens. BMC Neurosci. 2006, 7:49.
89. Zheng W.H., Quirion R. Comparative signaling pathways of insulin-like growth factor-1 and brain-derived neurotrophic factor in hippocampal neurons and the role of the PI3 kinase pathway in cell survival. J. Neurochem. 2004, 89:844-852.
90. Zhou J., Parada L.F. PTEN signaling in autism spectrum disorders. Curr. Opin. Neurobiol. 2012, 22:873-879.
91. Zhu Y., Hoell P., Ahlemeyer B., Krieglstein J. PTEN: a crucial mediator of mitochondria-dependent apoptosis. Apoptosis 2006, 11:197-207.