The neuroprotective effect of bone marrow stem cells is not dependent on direct cell contact with hypoxic injured tissue

Experimental Neurology

Volumn 215, Issue 2, 2009, Pages 317-327

  Sarnowska, Anna ^a,c   Braun, Holger ^b   Sauerzweig, Steven ^b   Reymann, Klaus G ^a,b  

^a FAN GmbH   (Germany)

^b LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^c POLISH ACADEMY OF SCIENCES   (Poland)

Author keywords

Bone marrow stem cells; Cortical primary culture; Hippocampal slice culture; Neuroprotection; Oxygen glucose deprivation; Serum deprivation; Stem cell therapy; Transplantation

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; NESTIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CONTACT; CELL CULTURE; CELL DIFFERENTIATION; CELL INTERACTION; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; HEMATOPOIETIC STEM CELL; HIPPOCAMPUS; HYPOXIA; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEM CELL TRANSPLANTATION; TISSUE INJURY;

ANIMALS; ANOXIA; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CELL DEATH; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; CEREBRAL CORTEX; COCULTURE TECHNIQUES; EMBRYO, MAMMALIAN; FLUORESCEINS; GENE EXPRESSION REGULATION; GLUCOSE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; NERVE TISSUE PROTEINS; NEURONS; ORGAN CULTURE TECHNIQUES; RATS; STEM CELLS;

EID: 58149512059     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.10.023     Document Type: Article

References (47)

1. Abe K. Therapeutic potential of neurotrophic factors and neural stem cells against ischemic brain injury. J. Cereb. Blood Flow Metab. 20 (2000) 1393-1408
2. Alvarez-Dolado M., Pardal R., Garcia-Verdugo J.M., Fike J.R., Lee H.O., Pfeffer K., Lois C., Morrison S.J., and Alvarez-Buylla A. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425 (2003) 968-973
3. Bonthius D.J., Karacay B., Dai D., and Pantazis N.J. FGF-2, NGF and IGF-1, but not BDNF, utilize a nitric oxide pathway to signal neurotrophic and neuroprotective effects against alcohol toxicity in cerebellar granule cell cultures. Brain Res. Dev. Brain Res. 140 (2003) 15-28
4. Braun H., Buhnemann C., Neumann J., and Reymann K.G. Preparation of a tissue-like cortical primary culture from embryonic rats using Matrigel and serum free Start V Medium. J. Neurosci. Methods 157 (2006) 32-38
5. Braun H., Buhnemann C., Neumann J., and Reymann K.G. Preparation of a tissue-like cortical primary culture from embryonic rats using Matrigel and serum free Start V Medium. J. Neurosci. Methods 157 (2006) 32-38
6. Buhnemann C., Scholz A., Bernreuther C., Malik C.Y., Braun H., Schachner M., Reymann K.G., and Dihne M. Neuronal differentiation of transplanted embryonic stem cell-derived precursors in stroke lesions of adult rats. Brain 129 (2006) 3238-3248
7. Cavaliere F., Dinkel K., and Reymann K. Microglia response and P2 receptor participation in oxygen/glucose deprivation-induced cortical damage. Neuroscience 136 (2005) 615-623
8. Chen X., Katakowski M., Li Y., Lu D., Wang L., Zhang L., Chen J., Xu Y., Gautam S., Mahmood A., and Chopp M. Human bone marrow stromal cell cultures conditioned by traumatic brain tissue extracts: growth factor production. J. Neurosci. Res. 69 (2002) 687-691
9. Chen X., Katakowski M., Li Y., Lu D., Wang L., Zhang L., Chen J., Xu Y., Gautam S., Mahmood A., and Chopp M. Human bone marrow stromal cell cultures conditioned by traumatic brain tissue extracts: growth factor production. J. Neurosci. Res. 69 (2002) 687-691
10. Chen X., Li Y., Wang L., Katakowski M., Zhang L., Chen J., Xu Y., Gautam S.C., and Chopp M. Ischemic rat brain extracts induce human marrow stromal cell growth factor production. Neuropathology 22 (2002) 275-279
11. Darsalia V., Heldmann U., Lindvall O., and Kokaia Z. Stroke-induced neurogenesis in aged brain. Stroke 36 (2005) 1790-1795
12. Dempsey, R.J., Kalluri, H.S. 2007. Ischemia-induced neurogenesis: role of growth factors. Neurosurg. Clin. N. Am. 18: 183-90, xi.
13. Dirnagl U., Iadecola C., and Moskowitz M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22 (1999) 391-397
14. Dluzniewska J., Sarnowska A., Beresewicz M., Johnson I., Srai S.K., Ramesh B., Goldspink G., Gorecki D.C., and Zablocka B. A strong neuroprotective effect of the autonomous C-terminal peptide of IGF-1 Ec (MGF) in brain ischemia. FASEB J. 19 (2005) 1896-1898
15. Golbs A., Heck N., and Luhmann H.J. A new technique for real-time analysis of caspase-3 dependent neuronal cell death. J. Neurosci. Methods 161 (2007) 234-243
16. Haynesworth S.E., Baber M.A., and Caplan A.I. Cytokine expression by human marrow-derived mesenchymal progenitor cells in vitro: effects of dexamethasone and IL-1 alpha. J. Cell Physiol. 166 (1996) 585-592
17. Jaworski J., Spangler S., Seeburg D.P., Hoogenraad C.C., and Sheng M. Control of dendritic arborization by the phosphoinositide-3'-kinase-Akt-mammalian target of rapamycin pathway. J. Neurosci. 25 (2005) 11300-11312
18. Jiang Y., Jahagirdar B.N., Reinhardt R.L., Schwartz R.E., Keene C.D., Ortiz-Gonzalez X.R., Reyes M., Lenvik T., Lund T., Blackstad M., Du J., Aldrich S., Lisberg A., Low W.C., Largaespada D.A., and Verfaillie C.M. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418 (2002) 41-49
19. Johnson-Farley N.N., Patel K., Kim D., and Cowen D.S. Interaction of FGF-2 with IGF-1 and BDNF in stimulating Akt, ERK, and neuronal survival in hippocampal cultures. Brain Res. 1154 (2007) 40-49 [Epub;%2007 Apr;%19]
20. Kokaia Z., and Lindvall O. Neurogenesis after ischaemic brain insults. Curr. Opin. Neurobiol. 13 (2003) 127-132
21. Kozlowska H., Jablonka J., Janowski M., Jurga M., Kossut M., and Domanska-Janik K. Transplantation of a novel human cord blood-derived neural-like stem cell line in a rat model of cortical infarct. Stem Cells Dev. 16 (2007) 481-488
22. Kozlowska H., Jablonka J., Janowski M., Jurga M., Kossut M., and Domanska-Janik K. Transplantation of a novel human cord blood-derived neural-like stem cell line in a rat model of cortical infarct. Stem Cells Dev. 16 (2007) 481-488
23. Kumar V., Zhang M.X., Swank M.W., Kunz J., and Wu G.Y. Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J. Neurosci. 25 (2005) 11288-11299
24. Lei Z., Ruan Y., Yang A.N., and Xu Z.C. NMDA receptor mediated dendritic plasticity in cortical cultures after oxygen-glucose deprivation. Neurosci. Lett. 407 (2006) 224-229
25. Li Y., Chen J., Chen X.G., Wang L., Gautam S.C., Xu Y.X., Katakowski M., Zhang L.J., Lu M., Janakiraman N., and Chopp M. Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery. Neurology 59 (2002) 514-523
26. Lindvall O., Kokaia Z., and Martinez-Serrano A. Stem cell therapy for human neurodegenerative disorders-how to make it work. Nat. Med. 10 Suppl. (2004) S42-S50
27. Liu Y., Dulchavsky D.S., Gao X., Kwon D., Chopp M., Dulchavsky S., and Gautam S.C. Wound repair by bone marrow stromal cells through growth factor production. J. Surg. Res. 136 (2006) 336-341
28. Lu J., Moochhala S., Moore X.L., Ng K.C., Tan M.H., Lee L.K., He B., Wong M.C., and Ling E.A. Adult bone marrow cells differentiate into neural phenotypes and improve functional recovery in rats following traumatic brain injury. Neurosci. Lett. 398 (2006) 12-17
29. Mahmood A., Lu D., and Chopp M. Intravenous administration of marrow stromal cells (MSCs) increases the expression of growth factors in rat brain after traumatic brain injury. J. Neurotrauma. 21 (2004) 33-39
30. Mahmood A., Lu D., and Chopp M. Marrow stromal cell transplantation after traumatic brain injury promotes cellular proliferation within the brain. Neurosurgery 55 (2004) 1185-1193
31. Mahmood A., Lu D., Qu C., Goussev A., and Chopp M. Human marrow stromal cell treatment provides long-lasting benefit after traumatic brain injury in rats. Neurosurgery 57 (2005) 1026-1031
32. Mahmood A., Lu D., Qu C., Goussev A., and Chopp M. Long-term recovery after bone marrow stromal cell treatment of traumatic brain injury in rats. J. Neurosurg. 104 (2006) 272-277
33. Neumann J., Gunzer M., Gutzeit H.O., Ullrich O., Reymann K.G., and Dinkel K. Microglia provide neuroprotection after ischemia. FASEB J. 20 (2006) 714-716
34. Nighoghossian N., Wiart M., Cakmak S., Berthezene Y., Derex L., Cho T.H., Nemoz C., Chapuis F., Tisserand G.L., Pialat J.B., Trouillas P., Froment J.C., and Hermier M. Inflammatory response after ischemic stroke: a USPIO-enhanced MRI study in patients. Stroke 38 (2007) 303-307
35. Ortiz-Gonzalez X.R., Keene C.D., Verfaillie C.M., and Low W.C. Neural induction of adult bone marrow and umbilical cord stem cells. Curr. Neurovasc. Res. 1 (2004) 207-213
36. Pforte C., Henrich-Noack P., Baldauf K., and Reymann K.G. Increase in proliferation and gliogenesis but decrease of early neurogenesis in the rat forebrain shortly after transient global ischemia. Neuroscience 136 (2005) 1133-1146
37. Pisati F., Bossolasco P., Meregalli M., Cova L., Belicchi M., Gavina M., Marchesi C., Calzarossa C., Soligo D., Lambertenghi-Deliliers G., Bresolin N., Silani V., Torrente Y., and Polli E. Induction of neurotrophin expression via human adult mesenchymal stem cells: implication for cell therapy in neurodegenerative diseases. Cell Transplant 16 (2007) 41-55
38. Pozzo Miller L.D., Mahanty N.K., Connor J.A., and Landis D.M. Spontaneous pyramidal cell death in organotypic slice cultures from rat hippocampus is prevented by glutamate receptor antagonists. Neuroscience 63 (1994) 471-487
39. Sanchez-Ramos J., Song S., Cardozo-Pelaez F., Hazzi C., Stedeford T., Willing A., Freeman T.B., Saporta S., Janssen W., Patel N., Cooper D.R., and Sanberg P.R. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp. Neurol. 164 (2000) 247-256
40. Sauerzweig, et al. A population of serumdeprivation-induced bone marrow stem cells (SD-BMSC) expresses marker typical for embryonic and neural stem cells. Exp. Cell Res. 315 1 (2009) 50-66 (Jan 1)
41. Schulman A. The search for alternative sources of human pluripotent stem cells. Stem Cell Rev. 1 (2005) 291-292
42. Steiner B., Klempin F., Wang L., Kott M., Kettenmann H., and Kempermann G. Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 54 (2006) 805-814
43. Stoppini L., Buchs P.A., and Muller D. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37 (1991) 173-182
44. Tabakman R., Jiang H., Shahar I., Arien-Zakay H., Levine R.A., and Lazarovici P. Neuroprotection by NGF in the PC12 in vitro OGD model: involvement of mitogen-activated protein kinases and gene expression. Ann. N. Y. Acad. Sci. 1053 (2005) 84-96
45. Zaman V., and Shetty A.K. Fetal hippocampal CA3 cell grafts enriched with fibroblast growth factor-2 exhibit enhanced neuronal integration into the lesioned aging rat hippocampus in a kainate model of temporal lobe epilepsy. Hippocampus 13 (2003) 618-632
46. Zaman V., and Shetty A.K. Pretreatment of donor cells with FGF-2 enhances survival of fetal hippocampal CA3 cell transplants in the chronically lesioned young adult hippocampus. Exp. Neurol. 183 (2003) 11-24
47. Zhang J., Li Y., Chen J., Yang M., Katakowski M., Lu M., and Chopp M. Expression of insulin-like growth factor 1 and receptor in ischemic rats treated with human marrow stromal cells. Brain Res. 1030 (2004) 19-27