Encapsulated Choroid Plexus Epithelial Cells Actively Protect Against Intrahippocampal Aβ-induced Long-Term Memory Dysfunction; Upregulation of Effective Neurogenesis with the Abrogated Apoptosis and Neuroinflammation

Journal of Molecular Neuroscience

Volumn 56, Issue 3, 2015, Pages 708-721

  Aliaghaei, Abbas ^a   Digaleh, Hadi ^a   Khodagholi, Fariba ^a   Ahmadiani, Abolhassan ^a,b  

^a SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b UNIVERSITY OF MALAYA   (Malaysia)

Author keywords

Alginate microcapsules; A ; Choroid plexus epithelial cells; Oxidative stress

Indexed keywords

ALGINIC ACID; BROXURIDINE; CASPASE 3; GLIAL FIBRILLARY ACIDIC PROTEIN; IONIZED CALCIUM BINDING ADAPTOR MOLECULE 1; PROTEIN; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; AMYLOID BETA PROTEIN; MICROCAPSULE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ENCAPSULATION; CELL MIGRATION; CHOROID PLEXUS; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; GLIOSIS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LONG TERM MEMORY; MALE; MEMORY DISORDER; MICROCAPSULE; MICROGLIA; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INFLAMMATION; NEUROEPITHELIUM CELL; NONHUMAN; RAT; TUNEL ASSAY; UPREGULATION; WESTERN BLOTTING; ANIMAL; CHEMISTRY; CYTOLOGY; EPITHELIUM CELL; MEMORY DISORDERS; PATHOLOGY; PATHOPHYSIOLOGY; TRANSPLANTATION; WISTAR RAT;

ALGINATES; AMYLOID BETA-PEPTIDES; ANIMALS; APOPTOSIS; CAPSULES; CHOROID PLEXUS; EPITHELIAL CELLS; HIPPOCAMPUS; MALE; MEMORY DISORDERS; MEMORY, LONG-TERM; NEUROGENESIS; RATS; RATS, WISTAR; UP-REGULATION;

EID: 84931570445     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-015-0492-y     Document Type: Article

References (55)

1. Adlard PA, Cummings BJ (2004) Alzheimer’s disease—a sum greater than its parts? Neurobiol Aging 25:725–733
2. Aliaghaei A, Khodagholi F, Ahmadiani A (2014) Conditioned media of choroid plexus epithelial cells induces Nrf2-activated phase II antioxidant response proteins and suppresses oxidative stress-induced apoptosis in PC12 cells. J Mol Neurosci 53(4):617–625
3. Aliev G (2011) Oxidative stress induced-metabolic imbalance, mitochondrial failure, and cellular hypoperfusion as primary pathogenetic factors for the development of Alzheimer disease which can be used as a alternate and successful drug treatment strategy: Past, present and future. CNS Neurol Disord Drug Targets 10:147–148
4. Awada R, Saulnier-Blache JS, Grès S, Bourdon E, Rondeau P, Parimisetty A, Orihuela R, Harry GJ, d’Hellencourt CL (2014) Autotaxin downregulates LPS-induced microglia activation and pro-inflammatory cytokines production. J Cell Biochem 115(12):2123–2132
5. Bailey P (1916) Morphology of the roof plate of the forebrain and the lateral choroid plexuses in the human embryo. J Comp Neurol 26:79–120
6. Baruch K, Ron-Harel N, Gal H, Deczkowska A, Shifrut E, Ndifon W, Mirlas-Neisberg N, Cardon M, Vaknin I, Cahalon L, Berkutzki T, Mattson MP, Gomez-Pinilla F, Friedman N, Schwartz M (2013) CNS-specific immunity at the choroid plexus shifts toward destructive Th2 inflammation in brain aging. Proc Natl Acad Sci U S A 110(6):2264–2269
7. Bates KA, Fonte J, Robertson TA, Martins RN, Harvey AR (2002) Chronic gliosis triggers Alzheimer’s disease-like processing of amyloid precursor protein. Neuroscience 113(4):785–796
8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
9. Bloom GS (2014) Amyloid-β and tau: the trigger and bullet in Alzheimer disease pathogenesis. JAMA Neurol 71(4):505–508
10. Bolos M, Spuch C, Ordoñez-Gutierrez L, Wandosell F, Ferrer I, Carro E (2013) Neurogenic effects of β-amyloid in the choroid plexus epithelial cells in Alzheimer’s disease. Cell Mol Life Sci 70(15):2787–2797
11. Bolos M, Antequera D, Aldudo J, Kristen H, Bullido MJ, Carro E (2014) Choroid plexus implants rescue Alzheimer’s disease-like pathologies by modulating amyloid-β degradation. Cell Mol Life Sci 71:2947–2955
12. Borlongan CV, Geaney M, Vasconcellos A, Elliott R, Skinner SS, Emerich DF, Borlongan CV (2004) Neuroprotection of striatal neurons by choroid plexus grafts in QA-lesioned rats. NeuroReport 15:2521–2525
13. Breteler MM, Claus JJ, van Duijn CM, Launer LJ, Hofman A (1992) Epidemiology of Alzheimer’s disease. Epidemiol Rev 14:59–82
14. Butterfield DA, Boyd-Kimball D (2004) Amyloid betapeptide(1–42) contributes to the oxidative stress and neurodegeneration found in Alzheimer disease brain. Brain Pathol 14:426–432
15. Calafiore M, Copani A, Deng W (2012) DNA polymerase-β mediates the neurogenic effect of β-amyloid protein in cultured subventricular zone neurospheres. J Neurosci Res 90:559–567
16. Chodobski A, Szmydynger-Chodobska J (2001) Choroid plexus: Target for polypeptides and site of their synthesis. Microsc Res Tech 52:65–82
17. Christen Y (2000) Oxidative stress and Alzheimer disease. Am J Clin Nutr 71:621S–629S
18. Diniz BS, Teixeira AL (2011) Brain-derived neurotrophic factor and Alzheimer’s disease: Physiopathology and beyond. Neuromol Med 13(4):217–222
19. Dionne KE, Cain BM, Li RH, Bell WJ, Doherty EJ, Rein DH, Lysaght MF, Gentile FT (1996) Transport characterization of membranes for immunoisolation. Biomaterials 17:257–266
20. Dohrmann GJ (1970) The choroid plexus: a historical review. Brain Res 18:197–218
21. Emerich DF, Orive G, Thanos C, Tornoe J, Walberg LU (2014) Encapsulated cell therapy for neurodegenerative diseases: from promise to product. Adv Drug Deliv Rev 67–68:131–141
22. Falk A, Frisén J (2002) Amphiregulin is a mitogen for adult neural stem cells. J Neurosci Res 69(6):757–762
23. Ferreiro E, Resende R, Costa R, Oliveira CR, Pereira CM (2006) An endoplasmic-reticulum-specific apoptotic pathway is involved in prion and amyloid-beta peptides neurotoxicity. Neurobiol Dis 23:669–678
24. Frackowiak J, Wisniewski HM, Wegiel J, Merz GS, Iqbal K, Wang KC (1992) Ultrastructure of the microglia that phagocytose amyloid and the microglia that produce beta-amyloid fibrils. Acta Neuropathol 84(3):225–233
25. Frautschy SA, Yang F, Irrizarry M, Hyman B, Saido TC, Hsiao K, Cole GM (1998) Microglial response to amyloid plaques in APPsw transgenic mice. Am J Pathol 152:307–317
26. Fu HJ, Liu B, Frost JL, Lemere CA (2010) Amyloid-beta immunotherapy for Alzheimer’s disease. CNS Neurol Disord Drug Targets 9(2):197–206
27. Hao T, Rockwell P (2013) Signaling through the vascular endothelial growth factor receptor VEGFR-2 protects hippocampal neurons from mitochondrial dysfunction and oxidative stress. Free Radic Biol Med 63:421–431
28. Haughey NJ, Liu D, Nath A, Borchard AC, Mattson MP (2002) Disruption of neurogenesis in the subventricular zone of adult mice, and in human cortical neuronal precursor cells in culture, by amyloid beta-peptide: Implications for the pathogenesis of Alzheimer’s disease. Neuromolecular. Neuromol Med 1(2):125–135
29. Jimenez S, Baglietto-Vargas D, Caballero C, Moreno-Gonzalez I, Torres M, Sanchez-Varo R, Ruano D, Vizuete M, Gutierrez A, Vitorica J (2008) Inflammatory response in the hippocampus of PS1M146L/APP751SL mouse model of Alzheimer's disease: age-dependent switch in the microglial phenotype from alternative to classic. J Neurosci 28:11650–61
30. Kakkar P, Das B, Viswanathan PN (1984) A modified spectrophotometric assay of superoxide dismutase. Ind J Biochem Biophys 21:130–132
31. Kihara T, Shimmyo Y, Akaike A, Niidome T, Sugimoto H (2010) Abeta-induced BACE-1 cleaves N-terminal sequence of mPGES- 2. Biochem Biophys Res Commun 393:728–733
32. Kimura K, Matsumoto N, Kitada M, Mizoguchi A, Ide C (2004) Neurite outgrowth from hippocampal neurons is promoted by choroid plexus ependymal cells in vitro. J Neurocytol 33(4):465–476
33. Kitazawa M, Yamasaki TR, LaFerla FM (2004) Microglia as a potential bridge between the amyloid beta-peptide and tau. Ann N Y Acad Sci 1035:85–103
34. Kweider N, Fragoulis A, Rosen C, Pecks U, Rath W, Pufe T, Wruck CJ (2011) Interplay between vascular endothelial growth factor (VEGF) and nuclear factor erythroid 2-related factor-2 (Nrf2): Implications for preeclampsia. J Biol Chem 286(50):42863–42872
35. Li Y, Chen J, Chopp M (2002) Cell proliferation and differentiation from ependymal, subependymal and choroid plexus cells in response to stroke in rats. J Neurosci Res 193:137–146
36. Li B, Zhong L, Yang X, Andersson T, Huang M, Tang SJ (2011) WNT5A signaling contributes to a beta-induced neuroinflammation and neurotoxicity. PLoS One 6:e22920
37. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443:787–795
38. Lindner MD, Kearns CE, Winn SR, Frydel BR, Emerich DF (1996) Effects of intraventricular encapsulated hNGF-secreting fibroblasts in aged rats. Cell Transplant 5:205–223
39. López-Toledano MA, Shelanski ML (2004) Neurogenic effect of beta-amyloid peptide in the development of neural stem cells. J Neurosci 24:5439–5444
40. Mandrekar-Colucci S, Landreth GE (2010) Microglia and inflammation in Alzheimer’s disease. CNS Neurol Disord: Drug Targets 9(2):156–167
41. Mimura J, Kosaka K, Maruyama A, Satoh T, Harada N, Yoshida H, Satoh K, Yamamoto M, Itoh K (2011) Nrf2 regulates NGF mRNA induction by carnosic acid in T98G glioblastoma cells and normal human astrocytes. J Biochem 150(2):209–217
42. Newman M, Musgrave IF, Lardelli M (2007) Alzheimer disease: Amyloidogenesis, the presenilins and animal models. Biochim Biophys Acta 1772:285–297
43. Numakawa T, Kumamaru E, Adachi N, Yagasaki Y, Izumi A, Kunugi H (2009) Glucocorticoid receptor interaction with TrkB promotes BDNF-triggered PLC-gamma signaling for glutamate release via a glutamate transporter. Proc Natl Acad Sci U S A 106(2):647–652
44. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates, 5th edn. Elsevier/Academic Press, Amsterdam
45. Perry G, Cash AD, Smith MA (2002) Alzheimer disease and oxidative stress. J Biomed Biotechnol 2(3):120–123
46. Rosales-Corral SA, Acuna-Castroviejo D, Coto-Montes A, Boga JA, Manchester LC, Fuentes-Broto L, Korkmaz A, Ma S, Tan DX, Reiter RJ (2012) Alzheimer’s disease: Pathological mechanisms and the beneficial role of melatonin. J Pineal Res 52:167–202
47. Russo I, Barlati S, Bosetti F (2011) Effects of neuroinflammation on the regenerative capacity of brain stem cells. J Neurochem 116(6):947–956
48. Salinas M, Diaz R, Abraham NG, de Galarreta CM R, Cuadrado A (2003) Nerve growth factor protects against 6-hydroxydopamine-induced oxidative stress by increasing expression of heme oxygenase-1 in a phosphatidylinositol 3-kinase-dependent manner. J Biol Chem 278(16):13898–13904
49. Speake T, Whitwell C, Kajita H, Majid A, Brown PD (2001) Mechanismsof CSF-secretion by the choroid plexus. Microsc Res Tech 52:49–59
50. Spuch C, Antequera D, Portero A, Orive G, Hernández RM, Molina JA, Bermejo-Pareja F, Pedraz JL, Carro E (2010) The effect of encapsulated VEGF-secreting cells on brain amyloid load and behavioral impairment in a mouse model of Alzheimer’s disease. Biomaterials 31(21):5608–5618
51. Tsay HJ, Wang P, Wang SL, Ku HH (2000) Age-associated changes of superoxide dismutase and catalase activities in the rat brain. J Biomed Sci 7(6):466–474
52. Watanabe Y, Matsumoto N, Dezawa M, Itokazu Y, Yoshihara T, Ide C (2005) Conditioned medium of the primary culture of rat choroid plexus epithelial (modified ependymal) cells enhances neurite outgrowth and survival of hippocampal neurons. Neurosci Lett 379:158–163
53. Williams WM, Castellani RJ, Weinberg A, Perry G, Smith MA (2012) Do β-defensins and other antimicrobial peptides play a role in neuroimmune function and neurodegeneration? Sci World J 19:1–11
54. Winn SR, Tresco PA (1994) Hydrogel applications for encapsulated cellular transplants. In: Flanagan TF, Emerich DF, Winn SR (eds) Methods in neuroscience, providing pharmacological access to the brain, vol 21. Academic, Orlando, pp 387–402
55. Zimmermann H, Shirley SG, Zimmermann U (2007) Alginate-based encapsulation of cells: Past, present, and future. Curr Diab Rep 7(4):314–320