Intracerebral adult stem cells transplantation increases brain-derived neurotrophic factor levels and protects against phencyclidine-induced social deficit in mice

Translational Psychiatry

Volumn 1, Issue , 2011, Pages

  Barzilay, R ^a   Ben Zur, T ^a   Sadan, O ^a   Bren, Z ^a   Taler, M ^a   Lev, N ^a   Tarasenko, I ^a   Uzan, R ^a   Gil Ad, I ^a   Melamed, E ^a   Weizman, A ^a   Offen, D ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

animal model; BDNF; phencyclidine; schizophrenia; social behavior; stem cells

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CLOZAPINE; PHENCYCLIDINE;

ADULT STEM CELL; ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BIOSYNTHESIS; DISEASE MODEL; DRUG EFFECT; HUMAN; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; METHODOLOGY; MOUSE; PHYSIOLOGY; PREFRONTAL CORTEX; SOCIAL BEHAVIOR; TRANSPLANTATION; UPREGULATION;

ADULT STEM CELLS; ANIMALS; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; CLOZAPINE; DISEASE MODELS, ANIMAL; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; PHENCYCLIDINE; PREFRONTAL CORTEX; SOCIAL BEHAVIOR; UP-REGULATION;

EID: 83755167954     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2011.64     Document Type: Article

References (57)

1. Lindvall O, Kokaia Z. Stem cells for the treatment of neurological disorders. Nature 2006; 441: 1094-1096. (Pubitemid 43990722)
2. Sadan O, Bahat-Stromza M, Barhum Y, Levy YS, Pisnevsky A, Peretz H et al. Protective effects of neurotrophic factors secreting cells in a 6-OHDA rat model of Parkinson disease. Stem Cells Dev 2009; 18: 1179-1190.
3. Barzilay R, Levy SY, Melamed E, Offen D. Adult stem cells for neuronal repair. Isr Med Assoc J 2006; 8: 61-66. (Pubitemid 43116072)
4. Tondreau T, Lagneaux L, Dejeneffe M, Massy M, Mortier C, Delforge A et al. Bone marrow derived mesenchymal stem cells already express specific neural proteins before any differentiation. Differentiation 2004; 72: 319-326. (Pubitemid 41702124)
5. Blondheim NR, Levy YS, Ben-Zur T, Burshtein A, Cherlow T, Kan I et al. Human mesenchymal stem cells express neural genes, suggesting a neural predisposition. Stem Cells Dev 2006; 15: 141-164. (Pubitemid 43726495)
6. Deng J, Petersen BE, Steindler DA, Jorgensen ML, Laywell ED. Mesenchymal stem cells spontaneously express neural proteins in culture and are neurogenic after transplantation. Stem Cells 2006; 24: 1054-1064.
7. Bahat-Stroomza M, Barhum Y, Levy YS, Karpov O, Bulvik S, Melamed E et al. Induction of adult human bone marrow mesenchymal stromal cells into functional astrocyte-like cells: Potential for restorative treatment in Parkinson's disease. J Mol Neurosc 2009; 39: 199-210.
8. Barhum Y, Gai Castro S, Bahat-Stroomza M, Barzilay R, Melamed E, Offen D. Intracerebroventricular transplantation of human mesenchymal stem cells induced to secrete neurotrophic factors attenuates clinical symptoms in a mouse model of multiple sclerosis. J Mol Neurosc 2010; 41: 129-137.
9. Hellmann MA, Panet H, Barhum Y, Melamed E, Offen D. Increased survival and migration of engrafted mesenchymal bone marrow stem cells in 6-hydroxydopamine-lesioned rodents. Neurosci Lett 2006; 395: 124-128. (Pubitemid 43188877)
10. Levy YS, Bahat-Stroomza M, Barzilay R, Burshtein A, Bulvik S, Barhum Y et al. Regenerative effect of neural-induced human mesenchymal stromal cells in rat models of Parkinson's disease. Cytotherapy 2008; 10: 340-352. (Pubitemid 351983158)
11. Offen D, Barhum Y, Levy YS, Burshtein A, Cherlow T, Melamed E. Intrastriatal transplantation of mouse bone marrow-derived stem cells improves motor behavior in a mouse model of Parkinson's disease. J Neural Transm Suppl 2007; 72: 133-143.
12. Sadan O, Shemesh N, Barzilay R, Bahat-Stromza M, Melamed E, Cohen Y et al. Migration of neurotrophic factors-secreting mesenchymal stem cells towards a quinolinic acid lesion as viewed by MRI. Stem Cells 2008; 26: 2542-2551.
13. Tfilin M, Sudai E, Merenlender A, Gispan I, Yadid G, Turgeman G. Mesenchymal stem cells increase hippocampal neurogenesis and counteract depressive-like behavior. Mol Psychiatr 2010; 15: 1164-1175.
14. Lieberman JA, Bymaster FP, Meltzer HY, Deutch AY, Duncan GE, Marx CE et al. Antipsychotic drugs: Comparison in animal models of efficacy, neurotransmitter regulation, and neuroprotection. Pharmacol Rev 2008; 60: 358-403.
15. Kantrowitz J, Javitt D. Thinking glutamatergically: Changing concepts of schizophrenia based upon changing neurochemical models. Clin Schizophr Relat Psychoses 2010; 4: 189-200.
16. Coyle JT. The glutamatergic dysfunction hypothesis for schizophrenia. Harv Rev Psychiatry 1996; 3: 241-253. (Pubitemid 26058365)
17. Durany N, Michel T, Zochling R, Boissl KW, Cruz-Sanchez FF, Riederer P et al. Brainderived neurotrophic factor and neurotrophin 3 in schizophrenic psychoses. Schizophr Res 2001; 52: 79-86. (Pubitemid 32947050)
18. Weickert CS, Hyde TM, Lipska BK, Herman MM, Weinberger DR, Kleinman JE. Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia. Mol Psychiatr 2003; 8: 592-610. (Pubitemid 36898018)
19. Arion D, Unger T, Lewis DA, Levitt P, Mirnics K. Molecular evidence for increased expression of genes related to immune and chaperone function in the prefrontal cortex in schizophrenia. Biol Psychiat 2007; 62: 711-721. (Pubitemid 47374650)
20. Eisch AJ, Cameron HA, Encinas JM, Meltzer LA, Ming GL, Overstreet-Wadiche LS. Adult neurogenesis, mental health, and mental illness: Hope or hype? J Neurosci 2008; 28: 11785-11791.
21. Ng F, Berk M, Dean O, Bush AI. Oxidative stress in psychiatric disorders: Evidence base and therapeutic implications. Int J Neuropsychoph 2008; 11: 851-876.
22. Rezin G, Amboni G, Zugno A, Quevedo J, Streck E. Mitochondrial dysfunction and psychiatric disorders. Neurochem Res 2009; 34: 1021-1029.
23. Lipska BK, Weinberger DR. To model a psychiatric disorder in animals: Schizophrenia as a reality test. Neuropsychopharmacol 2000; 23: 223-239. (Pubitemid 30609657)
24. Nestler EJ, Hyman SE. Animal models of neuropsychiatric disorders. Nat Neurosci 2010; 13: 1161-1169.
25. Amann LC, Gandal MJ, Halene TB, Ehrlichman RS, White SL, McCarren HS et al. Mouse behavioral endophenotypes for schizophrenia. Brain Res Bul 2010; 83: 147-161.
26. Nabeshima T, Mouri A, Murai R, Noda Y. Animal model of schizophrenia: Dysfunction of NMDA receptor-signaling in mice following withdrawal from repeated administration of phencyclidine. Ann NY Acad Sci 2006; 1086: 160-168. (Pubitemid 47084371)
27. Brigman JL, Ihne J, Sakisda LM, Bussey TJ, Holmes A. Effects of subchronic phencyclidine (PCP) treatment on social behaviors, and operant discrimination and reversal learning in C57BL/6J mice. Front Behav Neurosci 2009; 3: 2.
28. Ono T, Hashimoto E, Ukai W, Ishii T, Saito T. The role of neural stem cells for in vitro models of schizophrenia: Neuroprotection via Akt/ERK signal regulation. Schizophr Res 2010; 122: 239-247.
29. Nadler JJ, Moy SS, Dold G, Simmons N, Perez A, Young NB et al. Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav 2004; 3: 303-314. (Pubitemid 39277417)
30. Grunbaum-Novak N, Taler M, Gil-Ad I, Weizman A, Cohen H, Weizman R. Relationship between antidepressants and IGF-1 system in the brain: Possible role in cognition. Eur Neuropsychopharm 2008; 18: 431-438. (Pubitemid 351608552)
31. Taler M, Bar M, Korob I, Lomnitski L, Baharav E, Grunbaum-Novak N et al. Evidence for an inhibitory immunomodulatory effect of selected antidepressants on rat splenocytes: Possible relevance to depression and hyperactive-immune disorders. Int Immunopharmacol 2008; 8: 526-533.
32. Abbott A. Schizophrenia: The drug deadlock. Nature 2010; 468: 158-159.
33. Sadan O, Melamed E, Offen D. Bone-marrow-derived mesenchymal stem cell therapy for neurodegenerative diseases. Expert Opin Biol Th 2009; 9: 1487-1497.
34. Sensebe L, Krampera M, Schrezenmeier H, Bourin P, Giordano R. Mesenchymal stem cells for clinical application. Vox Sanguinis 2010; 98: 93-107.
35. Csernansky JG. Neurodegeneration in schizophrenia: Evidence from in vivo neuroimaging studies. ScientificWorldJournal 2007; 7: 135-143. (Pubitemid 46219352)
36. Jarskog LF, Miyamoto S, Lieberman JA. Schizophrenia: New pathological insights and therapies. Annu Rev Med 2007; 58: 49-61. (Pubitemid 46706500)
37. Do KQ, Cabungcal JH, Frank A, Steullet P, Cuenod M. Redox dysregulation, neurodevelopment, and schizophrenia. Curr Opin Neurobiol 2009; 19: 220-230.
38. Kassis I, Grigoriadis N, Gowda-Kurkalli B, Mizrachi-Kol R, Ben-Hur T, Slavin S et al. Neuroprotection and immunomodulation with mesenchymal stem cells in chronic experimental autoimmune encephalomyelitis. Arch Neurol 2008; 65: 753-761. (Pubitemid 351831453)
39. Rodrigues Hell RC, Silva Costa MM, Goes AM, Oliveira ALR. Local injection of BDNF producing mesenchymal stem cells increases neuronal survival and synaptic stability following ventral root avulsion. Neurobiol Dis 2009; 33: 290-300.
40. Shen LH, Li Y, Chopp M. Astrocytic endogenous glial cell derived neurotrophic factor production is enhanced by bone marrow stromal cell transplantation in the ischemic boundary zone after stroke in adult rats. Glia 2010; 58: 1074-1081.
41. Kan I, Barhum Y, Melamed E, Offen D. Mesenchymal stem cells stimulate endogenous neurogenesis in the subventricular zone of adult mice. Stem Cell Rev 2011; 7: 404-412.
42. Bao X, Wei J, Feng M, Lu S, Li G, Dou W et al. Transplantation of human bone marrowderived mesenchymal stem cells promotes behavioral recovery and endogenous neurogenesis after cerebral ischemia in rats. Brain Res 2011; 1367: 103-113.
43. Seillier A, Giuffrida A. Evaluation of NMDA receptor models of schizophrenia: Divergences in the behavioral effects of sub-chronic PCP and MK-801. Behav Brain Res 2009; 204: 410-415.
44. Schwabe K, Klein S, Koch M. Behavioural effects of neonatal lesions of the medial prefrontal cortex and subchronic pubertal treatment with phencyclidine of adult rats. Behav Brain Res 2006; 168: 150-160. (Pubitemid 43152063)
45. Wood JN. Social cognition and the prefrontal cortex. Behav Cogn Neurosci Rev 2003; 2: 97-114.
46. Qiao H, Noda Y, Kamei H, Nagai T, Furukawa H, Miura H et al. Clozapine, but not haloperidol, reverses social behavior deficit in mice during withdrawal from chronic phencyclidine treatment. Neuroreport 2001; 12: 11-16.
47. Prockop DJ. Repair of tissues by adult stem/progenitor cells (MSCs): Controversies, myths, and changing paradigms. Mol Ther 2009; 17: 939-946.
48. Sato Y, Takayanagi Y, Onaka T, Kobayashi E. Impact of cyclosporine upon emotional and social behavior in mice. Transplantation 2007; 83: 1365-1370. (Pubitemid 46800314)
49. Greenberg ME, Xu B, Lu B, Hempstead BL. New insights in the biology of BDNF synthesis and release: Implications in CNS function. J Neurosci 2009; 29: 12764-12767.
50. Cohen-Cory S, Kidane AH, Shirkey NJ, Marshak S. Brain-derived neurotrophic factor and the development of structural neuronal connectivity. Dev Neurobiol 2010; 70: 271-288.
51. Martinowich K, Manji H, Lu B. New insights into BDNF function in depression and anxiety. Nat Neurosci 2007; 10: 1089-1093. (Pubitemid 47339961)
52. Angelucci F, Brene S, Mathe AA. BDNF in schizophrenia, depression and corresponding animal models. Mol Psychiatr 2005; 10: 345-352.
53. Schaevitz LR, Moriuchi JM, Nag N, Mellot TJ, Berger-Sweeney J. Cognitive and social functions and growth factors in a mouse model of Rett syndrome. Physiol Behav 2010; 100: 255-263.
54. Broad KD, Mimmack ML, Keverne EB, Kendrick KM. Increased BDNF and trk-B mRNA expression in cortical and limbic regions following formation of a social recognition memory. Eur J Neurosci 2002; 16: 2166-2174. (Pubitemid 35454260)
55. Snigdha S, Neill J, McLean S, Shemar G, Cruise L, Shahid M et al. Phencyclidine (PCP)-induced disruption in cognitive performance is gender-specific and associated with a reduction in brain-derived neurotrophic factor (BDNF) in specific regions of the female rat brain. J Mol Neurosci 2011; 43: 337-345.
56. Prockop DJ, Kota DJ, Bazhanov N, Reger RL. Evolving paradigms for repair of tissues by adult stem/progenitor cells (MSCs). J Cell Mol Med 2010; 14: 2190-2199.
57. Xia Y, Wang CZ, Liu J, Anastasio NC, Johnson KM. Brain-derived neurotrophic factor prevents phencyclidine-induced apoptosis in developing brain by parallel activation of both the ERK and PI-3K/Akt pathways. Neuropharmacol 2010; 58: 330-336.