In vitro effects of fetal rat cerebrospinal fluid on viability and neuronal differentiation of PC12 cells

Fluids and Barriers of the CNS

Volumn 9, Issue 1, 2012, Pages

  Nabiuni, Mohammad ^a   Rasouli, Javad ^a   Parivar, Kazem ^b   Kochesfehani, Homa M ^a   Irian, Saeid ^a   Miyan, Jaleel A ^c  

^a KHARAZMI UNIVERSITY   (Iran)

^b ISLAMIC AZAD UNIVERSITY   (Iran)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Cerebrospinal fluid; Fetal rat; Neuronal differentiation; Pc12 cells

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; BETA TUBULIN; FIBROBLAST GROWTH FACTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ASSAY; CELL PROLIFERATION; CELL STRAIN; CELL VIABILITY; CEREBROSPINAL FLUID; CONTROLLED STUDY; CULTURE MEDIUM; FEMALE; FETUS; IMAGE ANALYSIS; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; MALE; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NERVE FIBER GROWTH; NEURITE; NONHUMAN; PRIMARY CELL CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

EID: 84863436535     PISSN: None     EISSN: 20458118     Source Type: Journal    
DOI: 10.1186/2045-8118-9-8     Document Type: Article

References (81)

1. Parvas M, Parada C, Bueno D. A blood-CSF barrier function controls embryonic CSF protein composition and homeostasis during early CNS development. Dev Biol 2008, 321:51-63. 10.1016/j.ydbio.2008.05.552, 18632096.
2. Gato A, Moro JA, Alonso MI, Bueno D, De La Mano A, Martin C. Embryonic cerebrospinal fluid regulates neuroepithelial survival, proliferation, and neurogenesis in chick embryos. Anat Rec A Discov Mol Cell Evol Biol 2005, 284A:475-484.
3. Parada C, Gato A, Bueno D. All-trans retinol and retinol-binding protein from embryonic cerebrospinal fluid exhibit dynamic behaviour during early central nervous system development. NeuroReport 2008, 19:945-950. 10.1097/WNR.0b013e3283021c94, 18520998.
4. Gato A, Desmond ME. Why the embryo still matters: CSF and the neuroepithelium as interdependent regulators of embryonic brain growth, morphogenesis and histiogenesis. Dev Biol 2009, 327:263-272. 10.1016/j.ydbio.2008.12.029, 19154733.
5. Martin C, Alonso MI, Santiago C, Moro JA, De la Mano A, Carretero R, Gato A. Early embryonic brain development in rats requires the trophic influence of cerebrospinal fluid. Int J Dev Neurosci 2009, 27:733-740. 10.1016/j.ijdevneu.2009.06.002, 19540909.
6. Miyan JA, Nabiyouni M, Zendah M. Development of the brain: a vital role for cerebrospinal fluid. Can J Physiol Pharmacol 2003, 81:317-328. 10.1139/y03-027, 12769224.
7. Pourghasem M, Mashayekhi F, Bannister CM, Miyan J. Changes in the csf fluid pathways in the developing rat fetus with early onset hydrocephalus. Eur J Pediatr Surg 2001, 11(Suppl 1):S10-S13.
8. Nabiyouni M, Storey C, Owen-Lynch J, Miyan J. Proteomics study of CSF composition in the developing H-Tx rat. Cerebrospinal Fluid Res 2004, 1:S29.
9. Parada C, Gato A, Aparicio M, Bueno D. Proteome analysis of chick embryonic cerebrospinal fluid. Proteomics 2006, 6:312-320. 10.1002/pmic.200500085, 16287170.
10. Mollanji R, Papaiconomou C, Boulton M, Midha R, Johnston M. Comparison of cerebrospinal fluid transport in fetal and adult sheep. Am J Physiol Regul Integr Comp Physiol 2001, 281:R1215-R1223.
11. Lehtinen MK, Walsh CA. Neurogenesis at the brain-cerebrospinal fluid interface. Annu Rev Cell Dev Biol 2011, 27:653-679. 10.1146/annurev-cellbio-092910-154026, 21801012.
12. Lehtinen MK, Zappaterra MW, Chen X, Yang YJ, Hill AD, Lun M, Maynard T, Gonzalez D, Kim S, Ye P, et al. The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron 2011, 69:893-905. 10.1016/j.neuron.2011.01.023, 3085909, 21382550.
13. Buddensiek J, Dressel A, Kowalski M, Runge U, Schroeder H, Hermann A, Kirsch M, Storch A, Sabolek M. Cerebrospinal fluid promotes survival and astroglial differentiation of adult human neural progenitor cells but inhibits proliferation and neuronal differentiation. BMC Neurosci 2010, 11:48. 10.1186/1471-2202-11-48, 2856586, 20377845.
14. Buddensiek J, Dressel A, Kowalski M, Storch A, Sabolek M. Adult cerebrospinal fluid inhibits neurogenesis but facilitates gliogenesis from fetal rat neural stem cells. J Neurosci Res 2009, 87:3054-3066. 10.1002/jnr.22150, 19530161.
15. Sawamoto K, Wichterle H, Gonzalez-Perez O, Cholfin JA, Yamada M, Spassky N, Murcia NS, Garcia-Verdugo JM, Marin O, Rubenstein JL, et al. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 2006, 311:629-632. 10.1126/science.1119133, 16410488.
16. Vigh B, Silva MJ ME, Frank CL, Vincze C, Czirok SJ, Szabo A, Lukats A, Szel A. The system of cerebrospinal fluid-contacting neurons. Its supposed role in the nonsynaptic signal transmission of the brain. Histol Histopathol 2004, 19:607-628.
17. Xia YX, Ikeda T, Xia XY, Ikenoue T. Differential neurotrophin levels in cerebrospinal fluid and their changes during development in newborn rat. Neurosci Lett 2000, 280:220-222. 10.1016/S0304-3940(00)00782-5, 10675800.
18. Rodriguez EM. The cerebrospinal fluid as a pathway in neuroendocrine integration. J Endocrinol 1976, 71:407-443. 10.1677/joe.0.0710407, 794431.
19. Miyan JA, Zendah M, Mashayekhi F, Owen-Lynch PJ. Cerebrospinal fluid supports viability and proliferation of cortical cells in vitro, mirroring in vivo development. Cerebrospinal Fluid Res 2006, 3:2. 10.1186/1743-8454-3-2, 1450312, 16549001.
20. Frye RE, Sequeira JM, Quadros EV, James SJ, Rossignol DA. Cerebral folate receptor autoantibodies in autism spectrum disorder. Mol Psychiatry 2012, Epub ahead of print.
21. Main PA, Angley MT, Thomas P, O'Doherty CE, Fenech M. Folate and methionine metabolism in autism: a systematic review. Am J Clin Nutr 2010, 91:1598-1620. 10.3945/ajcn.2009.29002, 20410097.
22. Moretti P, Sahoo T, Hyland K, Bottiglieri T, Peters S, del Gaudio D, Roa B, Curry S, Zhu H, Finnell RH, et al. Cerebral folate deficiency with developmental delay, autism, and response to folinic acid. Neurology 2005, 64:1088-1090. 10.1212/01.WNL.0000154641.08211.B7, 15781839.
23. Mashayekhi F, Draper CE, Bannister CM, Pourghasem M, Owen-Lynch PJ, Miyan JA. Deficient cortical development in the hydrocephalic Texas (H-Tx) rat: a role for CSF. Brain 2002, 125:1859-1874. 10.1093/brain/awf182, 12135976.
24. Owen-Lynch PJ, Draper CE, Mashayekhi F, Bannister CM, Miyan JA. Defective cell cycle control underlies abnormal cortical development in the hydrocephalic Texas rat. Brain 2003, 126:623-631. 10.1093/brain/awg058, 12566283.
25. Bannister CM, Nabiuni M, Zendah M, Mashayekhi F, Miyan JA. Development anomalies of the cerebral hemispheres in spina bifida aperta. Trends in Spina Bifida Research 2005, 31-42. Nova Science Publishers, Inc, New York, Zesta MR.
26. Cains S, Shepherd A, Nabiuni M, Owen-Lynch PJ, Miyan J. Addressing a folate imbalance in fetal cerebrospinal fluid can decrease the incidence of congenital hydrocephalus. J Neuropathol Exp Neurol 2009, 68:404-416. 10.1097/NEN.0b013e31819e64a7, 19287311.
27. Salehi Z, Mashayekhi F, Naji M, Pandamooz S. Insulin-like growth factor-1 and insulin-like growth factor binding proteins in cerebrospinal fluid during the development of mouse embryos. J Clin Neurosci 2009, 16:950-953. 10.1016/j.jocn.2008.09.018, 19359179.
28. Zougman A, Pilch B, Podtelejnikov A, Kiehntopf M, Schnabel C, Kumar C, Mann M. Integrated Analysis of the Cerebrospinal Fluid Peptidome and Proteome. J Proteome Res 2008, 7:386-399. 10.1021/pr070501k, 18052119.
29. Zappaterra MD, Lisgo SN, Lindsay S, Gygi SP, Walsh CA, Ballif BA. A comparative proteomic analysis of human and rat embryonic cerebrospinal fluid. J Proteome Res 2007, 6:3537-3548. 10.1021/pr070247w, 17696520.
30. Ek CJ, Dziegielewska KM, Habgood MD, Saunders NR. Barriers in the developing brain and Neurotoxicology. NeuroToxicology 2011, Epub ahead of print.
31. Ek CJ, Wong A, Liddelow SA, Johansson PA, Dziegielewska KM, Saunders NR. Efflux mechanisms at the developing brain barriers: ABC-transporters in the fetal and postnatal rat. Toxicol Lett 2010, 197:51-59. 10.1016/j.toxlet.2010.04.025, 20466047.
32. Saunders NR, Habgood MD, Dziegielewska KM. Barrier mechanisms in the brain, I. Adult brain. Clin Exp Pharmacol Physiol 1999, 26:11-19. 10.1046/j.1440-1681.1999.02986.x, 10027064.
33. Saunders NR, Habgood MD, Dziegielewska KM. Barrier mechanisms in the brain, II. Immature brain. Clin Exp Pharmacol Physiol 1999, 26:85-91. 10.1046/j.1440-1681.1999.02987.x, 10065326.
34. Holman DW, Kurtcuoglu V, Grzybowski DM. Cerebrospinal fluid dynamics in the human cranial subarachnoid space: an overlooked mediator of cerebral disease. II. In vitro arachnoid outflow model. J R Soc Interface 2010, 7:1205-1218. 10.1098/rsif.2010.0032, 2894876, 20335192.
35. Gupta S, Soellinger M, Grzybowski DM, Boesiger P, Biddiscombe J, Poulikakos D, Kurtcuoglu V. Cerebrospinal fluid dynamics in the human cranial subarachnoid space: an overlooked mediator of cerebral disease. I. Computational model. J R Soc Interface 2010, 7:1195-1204. 10.1098/rsif.2010.0033, 2894877, 20236960.
36. Koh L, Nagra G, Johnston M. Properties of the lymphatic cerebrospinal fluid transport system in the rat: impact of elevated intracranial pressure. J Vasc Res 2007, 44:423-432. 10.1159/000104255, 17587862.
37. Koh L, Zakharov A, Nagra G, Armstrong D, Friendship R, Johnston M. Development of cerebrospinal fluid absorption sites in the pig and rat: connections between the subarachnoid space and lymphatic vessels in the olfactory turbinates. Anat Embryol (Berl) 2006, 211:335-344.
38. Koh L, Zakharov A, Johnston M. Integration of the subarachnoid space and lymphatics: is it time to embrace a new concept of cerebrospinal fluid absorption?. Cerebrospinal Fluid Res 2005, 2:6. 10.1186/1743-8454-2-6, 1266390, 16174293.
39. Perez-Figares JM, Jimenez AJ, Rodriguez EM. Subcommissural organ, cerebrospinal fluid circulation, and hydrocephalus. Microsc Res Tech 2001, 52:591-607. 10.1002/1097-0029(20010301)52:5<591::AID-JEMT1043>3.0.CO;2-7, 11241868.
40. Nicholson C. Signals that go with the flow. rends Neurosci 1999, 22:143-145.
41. D'Alessandro R, Meldolesi J. In PC12 cells, expression of neurosecretion and neurite outgrowth are governed by the transcription repressor REST/NRSF. Cell Mol Neurobiol 2010, 30:1295-1302. 10.1007/s10571-010-9602-0, 21046448.
42. Martin TF, Grishanin RN. PC12 cells as a model for studies of regulated secretion in neuronal and endocrine cells. Methods Cell Biol 2003, 71:267-286.
43. Vaudry D, Chen Y, Hsu CM, Eiden LE. PC12 cells as a model to study the neurotrophic activities of PACAP. Ann N Y Acad Sci 2002, 971:491-496. 10.1111/j.1749-6632.2002.tb04513.x, 12438169.
44. Fujita K, Lazarovici P, Guroff G. Regulation of the differentiation of PC12 pheochromocytoma cells. Environ Health Perspect 1989, 80:127-142. 1567620, 2647474.
45. Guerrini R, Dobyns WB, Barkovich AJ. Abnormal development of the human cerebral cortex: genetics, functional consequences and treatment options. Trends Neurosci 2008, 31:154-162. 10.1016/j.tins.2007.12.004, 18262290.
46. Rakic P. A century of progress in corticoneurogenesis: from silver impregnation to genetic engineering. Cereb Cortex 2006, 16(Suppl 1):i3-17.
47. Chen RL, Kassem NA, Redzic ZB, Chen CP, Segal MB, Preston JE. Age-related changes in choroid plexus and blood-cerebrospinal fluid barrier function in the sheep. Exp Gerontol 2009, 44:289-296. 10.1016/j.exger.2008.12.004, 19133323.
48. Redzic ZB, Preston JE, Duncan JA, Chodobski A, Szmydynger-Chodobska J. The choroid plexus-cerebrospinal fluid system: from development to aging. Curr Top Dev Biol 2005, 71:1-52.
49. Meiniel A. The secretory ependymal cells of the subcommissural organ: which role in hydrocephalus?. Int J Biochem Cell Biol 2007, 39:463-468. 10.1016/j.biocel.2006.10.021, 17150405.
50. Picketts DJ. Neuropeptide signaling and hydrocephalus: SCO with the flow. J Clin Invest 2006, 116:1828-1832. 10.1172/JCI29148, 1483144, 16823482.
51. Somera KC, Jones HC. Reduced subcommissural organ glycoprotein immunoreactivity precedes aqueduct closure and ventricular dilatation in H-Tx rat hydrocephalus. Cell Tissue Res 2004, 315:361-373. 10.1007/s00441-003-0843-9, 14722750.
52. Caprile T, Hein S, Rodriguez S, Montecinos H, Rodriguez E. Reissner fiber binds and transports away monoamines present in the cerebrospinal fluid. Brain Res Mol Brain Res 2003, 110:177-192.
53. Somera KC, Jones H. Subcommissural organ dysfunction in H-Tx rats with early-onset hydrocephalus. Eur J Pediatr Surg 2002, 12(Suppl 1):S45-47.
54. Rodriguez E, Yulis CR. Subcommissural organ. Cellular, molecular, physiological, and pathological aspects: one hundred years of subcommissural organ research. Microsc Res Tech 2001, 52:459-460. 10.1002/1097-0029(20010301)52:5<459::AID-JEMT1031>3.0.CO;2-Y, 11241856.
55. Salehi Z, Mashayekhi F. The role of cerebrospinal fluid on neural cell survival in the developing chick cerebral cortex: an in vivo study. Eur J Neurol 2006, 13:760-764. 10.1111/j.1468-1331.2006.01358.x, 16834707.
56. Sankaranarayani R, Nalini A, Rao Laxmi T, Raju TR. Altered neuronal activities in the motor cortex with impaired motor performance in adult rats observed after infusion of cerebrospinal fluid from amyotrophic lateral sclerosis patients. Behav Brain Res 2010, 206:109-119. 10.1016/j.bbr.2009.09.009, 19747511.
57. Steinfeld R, Grapp M, Kraetzner R, Dreha-Kulaczewski S, Helms G, Dechent P, Wevers R, Grosso S, Gartner J. Folate receptor alpha defect causes cerebral folate transport deficiency: a treatable neurodegenerative disorder associated with disturbed myelin metabolism. Am J Hum Genet 2009, 85:354-363. 10.1016/j.ajhg.2009.08.005, 2771535, 19732866.
58. Parada C, Escola-Gil JC, Bueno D. Low-density lipoproteins from embryonic cerebrospinal fluid are required for neural differentiation. J Neurosci Res 2008, 86:2674-2684. 10.1002/jnr.21724, 18500757.
59. Juranek J, Fletcher JM, Hasan KM, Breier JI, Cirino PT, Pazo-Alvarez P, Diaz JD, Ewing-Cobbs L, Dennis M, Papanicolaou AC. Neocortical reorganization in spina bifida. NeuroImage 2008, 40:1516-1522. 10.1016/j.neuroimage.2008.01.043, 2410089, 18337124.
60. Bachy I, Kozyraki R, Wassef M. The particles of the embryonic cerebrospinal fluid: How could they influence brain development?. Brain Res Bull 2008, 75:289-294. 10.1016/j.brainresbull.2007.10.010, 18331886.
61. Mercimek-Mahmutoglu S, Stockler-Ipsiroglu S. Cerebral folate deficiency and folinic acid treatment in hypomyelination with atrophy of the basal ganglia and cerebellum (H-ABC) syndrome. Tohoku J Exp Med 2007, 211:95-96. author reply 97, 10.1620/tjem.211.95, 17202777.
62. y ValenzuelaI M-P, Carmona-Calero EM, Perez-Gonzalez H, Ormazabal-Ramos C, Fernandez-Rodriguez P, Gonzalez-Marrero I, Castaneyra-Perdomo A, Ferres-Torres R. Alterations of the cerebrospinal fluid proteins and subcommissural organ secretion in the arterial hypertension and ventricular dilatation. A study in SHR rats. Histol Histopathol 2006, 21:179-185.
63. Khwaja FW, Nolen JD, Mendrinos SE, Lewis MM, Olson JJ, Pohl J, Van Meir EG, Ritchie JC, Brat DJ. Proteomic analysis of cerebrospinal fluid discriminates malignant and nonmalignant disease of the central nervous system and identifies specific protein markers. Proteomics 2006, 6:6277-6287. 10.1002/pmic.200600135, 17078017.
64. Huhmer AF, Biringer RG, Amato H, Fonteh AN, Harrington MG. Protein analysis in human cerebrospinal fluid: Physiological aspects, current progress and future challenges. Dis Markers 2006, 22:3-26.
65. Zhang J, Goodlett DR, Peskind ER, Quinn JF, Zhou Y, Wang Q, Pan C, Yi E, Eng J, Aebersold RH, Montine TJ. Quantitative proteomic analysis of age-related changes in human cerebrospinal fluid. Neurobiol Aging 2005, 26:207-227. 10.1016/j.neurobiolaging.2004.03.012, 15582749.
66. Yuan X, Desiderio DM. Proteomics analysis of human cerebrospinal fluid. J Chromatogr B Analyt Technol Biomed Life Sci 2005, 815:179-189. 10.1016/j.jchromb.2004.06.044, 15652808.
67. Dziegielewska KM, Knott GW, Saunders NR. The nature and composition of the internal environment of the developing brain. Cell Mol Neurobiol 2000, 20:41-56. 10.1023/A:1006943926765, 10690501.
68. Johanson CE, Duncan JA, Klinge PM, Brinker T, Stopa EG, Silverberg GD. Multiplicity of cerebrospinal fluid functions: New challenges in health and disease. Cerebrospinal Fluid Res 2008, 5:10. 10.1186/1743-8454-5-10, 2412840, 18479516.
69. Martin C, Bueno D, Alonso MI, Moro JA, Callejo S, Parada C, Martin P, Carnicero E, Gato A. FGF2 plays a key role in embryonic cerebrospinal fluid trophic properties over chick embryo neuroepithelial stem cells. Dev Biol 2006, 297:402-416. 10.1016/j.ydbio.2006.05.010, 16916506.
70. Mashayekhi F, Azari M, Moghadam LM, Yazdankhah M, Naji M, Salehi Z. Changes in cerebrospinal fluid nerve growth factor levels during chick embryonic development. J Clin Neurosci 2009,
71. Mashayekhi F. Neural cell death is induced by neutralizing antibody to nerve growth factor: an in vivo study. Brain Dev 2008, 30:112-117. 10.1016/j.braindev.2007.07.001, 17706905.
72. Gordon N. Cerebral folate deficiency. Dev Med Child Neurol 2009, 51:180-182. 10.1111/j.1469-8749.2008.03185.x, 19260931.
73. Ramaekers VT, Sequeira JM, Blau N, Quadros EV. A milk-free diet downregulates folate receptor autoimmunity in cerebral folate deficiency syndrome. Dev Med Child Neurol 2008, 50:346-352. 10.1111/j.1469-8749.2008.02053.x, 2715943, 18355335.
74. Ramaekers VT, Weis J, Sequeira JM, Quadros EV, Blau N. Mitochondrial complex I encephalomyopathy and cerebral 5-methyltetrahydrofolate deficiency. Neuropediatrics 2007, 38:184-187. 10.1055/s-2007-991150, 18058625.
75. Ramaekers VT, Sequeira JM, Artuch R, Blau N, Temudo T, Ormazabal A, Pineda M, Aracil A, Roelens F, Laccone F, Quadros EV. Folate receptor autoantibodies and spinal fluid 5-methyltetrahydrofolate deficiency in rett syndrome. Neuropediatrics 2007, 38:179-183. 10.1055/s-2007-991148, 18058624.
76. Ramaekers VT, Blau N, Sequeira JM, Nassogne MC, Quadros EV. Folate receptor autoimmunity and cerebral folate deficiency in low-functioning autism with neurological deficits. Neuropediatrics 2007, 38:276-281. 10.1055/s-2008-1065354, 18461502.
77. Koenig MK, Perez M, Rothenberg S, Butler IJ. Juvenile onset central nervous system folate deficiency and rheumatoid arthritis. J Child Neurol 2008, 23:106-107. 3072705, 18056694.
78. Pineda M, Ormazabal A, Lopez-Gallardo E, Nascimento A, Solano A, Herrero MD, Vilaseca MA, Briones P, Ibanez L, Montoya J, Artuch R. Cerebral folate deficiency and leukoencephalopathy caused by a mitochondrial DNA deletion. Ann Neurol 2006, 59:394-398. 10.1002/ana.20746, 16365882.
79. Willemsen MA, Wevers RA, Verbeek MM. Cerebral folate deficiency syndrome. N Engl J Med 2005, 353:740. author reply.
80. Hansen FJ, Blau N. Cerebral folate deficiency: life-changing supplementation with folinic acid. Mol Genet Metab 2005, 84:371-373. 10.1016/j.ymgme.2004.12.001, 15781200.
81. Ramaekers VT, Blau N. Cerebral folate deficiency. Dev Med Child Neurol 2004, 46:843-851.