Autophagy has a key role in the pathophysiology of schizophrenia

Molecular Psychiatry

Volumn 20, Issue 1, 2015, Pages 126-132

  Merenlender Wagner, A ^a   Malishkevich, A ^a   Shemer, Z ^a   Udawela, M ^b   Gibbons, A ^b   Scarr, E ^b   Dean, B ^b   Levine, J ^c,d   Agam, G ^c,d,e   Gozes, I ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c Psychiatry Research Unit   (Israel)

^d MENTAL HEALTH CENTER   (Israel)

^e BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY DEPENDENT NEUROPROTECTIVE PROTEIN; ACTIVITY DEPENDENT NEUROPROTECTIVE PROTEIN 2; BECLIN 1; CLOZAPINE; PROTEIN; UNCLASSIFIED DRUG; ADNP PROTEIN, HUMAN; APOPTOSIS REGULATORY PROTEIN; BECN1 PROTEIN, RAT; HOMEODOMAIN PROTEIN; MAP1LC3 PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; NERVE PROTEIN; NEUROLEPTIC AGENT; PROTEIN BAD;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; LYMPHOCYTE; MALE; MOUSE; NERVE CELL NECROSIS; NONHUMAN; PATHOPHYSIOLOGY; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCHIZOPHRENIA; SOCIAL DISABILITY; ADULT; AGED; ANIMAL; CASE CONTROL STUDY; DEFICIENCY; DRUG EFFECTS; ETHICS; FEMALE; GENETICS; HIPPOCAMPUS; KNOCKOUT MOUSE; METABOLISM; MIDDLE AGED; NEUROBLASTOMA; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TRANSFORMED CELL LINE; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIPSYCHOTIC AGENTS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BCL-ASSOCIATED DEATH PROTEIN; CASE-CONTROL STUDIES; CELL LINE, TRANSFORMED; CLOZAPINE; FEMALE; HIPPOCAMPUS; HOMEODOMAIN PROTEINS; HUMANS; LYMPHOCYTES; MALE; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MIDDLE AGED; NERVE TISSUE PROTEINS; NEUROBLASTOMA; RATS; RATS, SPRAGUE-DAWLEY; SCHIZOPHRENIA; YOUNG ADULT;

EID: 84922219094     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2013.174     Document Type: Article

References (50)

1. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T et al. The role of autophagy during the early neonatal starvation period. Nature 2004; 432: 1032-1036.
2. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006; 441: 885-889.
3. Mortensen M, Ferguson DJ, Edelmann M, Kessler B, Morten KJ, Komatsu M et al. Loss of autophagy in erythroid cells leads to defective removal of mitochondria and severe anemia in vivo. Proc Natl Acad Sci USA 2010; 107: 832-837.
4. Debnath J, Baehrecke EH, Kroemer G. Does autophagy contribute to cell death? Autophagy 2005; 1: 66-74.
5. Lum JJ, Bauer DE, Kong M, Harris MH, Li C, Lindsten T et al. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 2005; 120: 237-248.
6. Lieberman JA. Is schizophrenia a neurodegenerative disorder? A clinical and neurobiological perspective. Biol Psychiatry 1999; 46: 729-739.
7. Benes FM, Kwok EW, Vincent SL, Todtenkopf MS. A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressives. Biol Psychiatry 1998; 44: 88-97.
8. Glantz LA, Gilmore JH, Lieberman JA, Jarskog LF. Apoptotic mechanisms and the synaptic pathology of schizophrenia. Schizophr Res 2006; 81: 47-63.
9. Cao Y, Klionsky DJ. Physiological functions of Atg6/Beclin 1: a unique autophagyrelated protein. Cell Res 2007; 17: 839-849.
10. Sun Q, Fan W, Zhong Q. Regulation of Beclin 1 in autophagy. Autophagy 2009; 5: 713-716.
11. Yue Z, Jin S, Yang C, Levine AJ, Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci U S A 2003; 100: 15077-15082.
12. Wang J. Beclin 1 bridges autophagy, apoptosis and differentiation. Autophagy 2008; 4: 947-948.
13. Kim M, Fekadu J, Maronde E, Rami A. Alleviation of autophagy by knockdown of Beclin-1 enhances susceptibility of hippocampal neurons to proapoptotic signals induced by amino acid starvation. Histochem Cell Biol 2013; 139: 99-108.
14. Homma K, Suzuki K, Sugawara H. The Autophagy Database: an all-inclusive information resource on autophagy that provides nourishment for research. Nucleic Acids Res 2011; 39: D986-D990.
15. Wu J, Dang Y, Su W, Liu C, Ma H, Shan Y et al. Molecular cloning and characterization of rat LC3A and LC3B-two novel markers of autophagosome. Biochem Biophys Res Commun 2006; 339: 437-442.
16. Mizushima N. Autophagy: process and function. Genes Dev 2007; 21: 2861-2873.
17. Vinayagam A, Stelzl U, Foulle R, Plassmann S, Zenkner M, Timm J et al. A directed protein interaction network for investigating intracellular signal transduction. Sci Signal 2011; 4: rs8.
18. Bassan M, Zamostiano R, Davidson A, Pinhasov A, Giladi E, Perl O et al. Complete sequence of a novel protein containing a femtomolar-activity-dependent neuroprotective peptide. J Neurochem 1999; 72: 1283-1293.
19. Kushnir M, Dresner E, Mandel S, Gozes I. Silencing of the ADNP-family member, ADNP2, results in changes in cellular viability under oxidative stress. J Neurochem 2008; 105: 537-545.
20. Sigalov E, Fridkin M, Brenneman DE, Gozes I. VIP-Related protection against lodoacetate toxicity in pheochromocytoma (PC12) cells: a model for ischemic/ hypoxic injury. J Mol Neurosci 2000; 15: 147-154.
21. Zamostiano R, Pinhasov A, Gelber E, Steingart RA, Seroussi E, Giladi E et al. Cloning and characterization of the human activity-dependent neuroprotective protein. J Biol Chem 2001; 276: 708-714.
22. Mandel S, Gozes I. Activity-dependent neuroprotective protein constitutes a novel element in the SWI/SNF chromatin remodeling complex. J Biol Chem 2007; 282: 34448-34456.
23. Pinhasov A, Mandel S, Torchinsky A, Giladi E, Pittel Z, Goldsweig AM et al. Activitydependent neuroprotective protein: a novel gene essential for brain formation. Brain Res Dev Brain Res 2003; 144: 83-90.
24. Mandel S, Rechavi G, Gozes I. Activity-dependent neuroprotective protein (ADNP) differentially interacts with chromatin to regulate genes essential for embryogenesis. Dev Biol 2007; 303: 814-824.
25. Vulih-Shultzman I, Pinhasov A, Mandel S, Grigoriadis N, Touloumi O, Pittel Z et al. Activity-dependent neuroprotective protein snippet NAP reduces tau hyperphosphorylation and enhances learning in a novel transgenic mouse model. J Pharmacol Exp Ther 2007; 323: 438-449.
26. Mandel S, Spivak-Pohis I, Gozes I. ADNP differential nucleus/cytoplasm localization in neurons suggests multiple roles in neuronal differentiation and maintenance. J Mol Neurosci 2008; 35: 127-141.
27. Furman S, Steingart RA, Mandel S, Hauser JM, Brenneman DE, Gozes I. Subcellular localization and secretion of activity-dependent neuroprotective protein in astrocytes. Neuron Glia Biol 2004; 1: 193-199.
28. Dresner E, Malishkevich A, Arviv C, Leibman Barak S, Alon S, Ofir R et al. Novel Evolutionary-conserved Role for the Activity-dependent Neuroprotective Protein (ADNP) Family That Is Important for Erythropoiesis. J Biol Chem 2012; 287: 40173-40185.
29. Steingart RA, Gozes I. Recombinant activity-dependent neuroprotective protein protects cells against oxidative stress. Mol Cell Endocrinol 2006; 252: 148-153.
30. Divinski I, Mittelman L, Gozes I. A femtomolar acting octapeptide interacts with tubulin and protects astrocytes against zinc intoxication. J Biol Chem 2004; 279: 28531-28538.
31. Khandhadia S, Cherry J, Lotety AJ. Age-Related Macular Degeneration. Neurodegener Diseases In: Ahmad SI, Landes Bioscience + Business Media (eds). 2012; Chapter 2, pp 15-36.
32. Gozes I, Steingart RA, Spier AD. NAP mechanisms of neuroprotection. J Mol Neurosci 2004; 24: pp67-72.
33. Leker RR, Teichner A, Grigoriadis N, Ovadia H, Brenneman DE, Fridkin M et al. NAP, a femtomolar-acting peptide, protects the brain against ischemic injury by reducing apoptotic death. Stroke 2002; 33: 1085-1092.
34. Idan-Feldman A, Ostritsky R, Gozes I. Tau and caspase 3 as targets for neuroprotection. Int J Alzheimers Dis 2012; 2012: 493670.
35. Idan-Feldman A, Schirer Y, Polyzoidou E, Touloumi O, Lagoudaki R, Grigoriadis NC et al. Davunetide (NAP) as a preventative treatment for central nervous system complications in a diabetes rat model. Neurobiol Dis 2011; 44: 327-339.
36. Zemlyak I, Sapolsky R, Gozes I. NAP protects against cytochrome c release: inhibition of the initiation of apoptosis. Eur J Pharmacol 2009; 618: 9-14.
37. Zemlyak I, Manley N, Sapolsky R, Gozes I. NAP protects hippocampal neurons against multiple toxins. Peptides 2007; 28: 2004-2008.
38. Dresner E, Agam G, Gozes I. Activity-dependent neuroprotective protein (ADNP) expression level is correlated with the expression of the sister protein ADNP2: deregulation in schizophrenia. Eur Neuropsychopharmacol 2011; 21: 355-361.
39. Merenlender-Wagner A, Pikman R, Giladi E, Andrieux A, Gozes I. NAP (davunetide) enhances cognitive behavior in the STOP heterozygous mousea microtubuledeficient model of schizophrenia. Peptides 2010; 31: 1368-1373.
40. Javitt DC, Buchanan RW, Keefe RS, Kern R, McMahon RP, Green MF et al. Effect of the neuroprotective peptide davunetide (AL-108) on cognition and functional capacity in schizophrenia. Schizophr Res 2012; 136: 25-31.
41. Jarskog LF, Dong Z, Kangarlu A, Colibazzi T, Girgis RR, Kegeles LS et al. Effects of davunetide on N-acetylaspartate and choline in dorsolateral prefrontal cortex in patients with schizophrenia. Neuropsychopharmacology 2013; 38: 1245-1252.
42. Erlich S, Mizrachy L, Segev O, Lindenboim L, Zmira O, Adi-Harel S et al. Differential interactions between Beclin 1 and Bcl-2 family members. Autophagy 2007; 3: 561-568.
43. Kozlovsky N, Nadri C, Belmaker RH, Agam G. Lack of effect of mood stabilizers or neuroleptics on GSK-3 protein levels and GSK-3 activity. Int J Neuropsychopharmacol 2003; 6: 117-120.
44. Zink M, Schmitt A, May B, Muller B, Demirakca T, Braus DF et al. Differential effects of long-term treatment with clozapine or haloperidol on GABAA receptor binding and GAD67 expression. Schizophr Res 2004; 66: 151-157.
45. Dresner E, Agam G, Gozes I. Activity-dependent neuroprotective protein (ADNP) expression level is correlated with the expression of the sister protein ADNP2: Deregulation in schizophrenia. Eur Neuropsychopharmacol 2011; 21: 355-361.
46. Furman S, Hill JM, Vulih I, Zaltzman R, Hauser JM, Brenneman DE et al. Sexual dimorphism of activity-dependent neuroprotective protein in the mouse arcuate nucleus. Neurosci Lett 2005; 373: 73-78.
47. Begemann MJ, Dekker CF, van Lunenburg M, Sommer IE. Estrogen augmentation in schizophrenia: a quantitative review of current evidence. Schizophr Res 2012; 141: 179-184.
48. Ben-David E, Shifman S. Combined analysis of exome sequencing points toward a major role for transcription regulation during brain development in autism. Mol Psychiatry 2013; 18: 1054-1056.
49. Schaeffer V, Lavenir I, Ozcelik S, Tolnay M, Winkler DT, Goedert M. Stimulation of autophagy reduces neurodegeneration in a mouse model of human tauopathy. Brain 2012; 135(Pt 7): 2169-2177.
50. Esteves AR, Gozes I, Cardoso SM. The rescue of microtubule-dependent traffic recovers mitochondrial function in Parkinson's disease. Biochim Biophys Acta 2013; 1842: 7-21.