Human mesenchymal stromal cells and their derivative, SB623 cells, rescue neural cells via trophic support following in vitro ischemia

Cell Transplantation

Volumn 19, Issue 8, 2010, Pages 973-984

  Tate, Ciara C ^a   Fonck, Carlos ^a   McGrogan, Michael ^a   Case, Casey C ^a  

^a SanBio Inc   (United States)

Author keywords

Cerebral ischemia; Mesenchymal stromal cells; Oxygen glucose deprivation; SB623 cells; Trophic support

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN ISCHEMIA; CELL CONTACT; CELL DAMAGE; CYTOKINE RELEASE; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MESENCHYMAL STEM CELL; MESENCHYMAL STROMA CELL; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SB623 CELL; STROMA CELL;

ADULT; BONE MARROW CELLS; BRAIN ISCHEMIA; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; HIPPOCAMPUS; HUMANS; MESENCHYMAL STEM CELLS; NERVE GROWTH FACTORS; NEURONS;

EID: 78349248603     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368910X494885     Document Type: Article

References (45)

1. Aizman, I.; Tate, C. C.; McGrogan, M.; Case, C. C. Extracellular matrix produced by bone marrow stromal cells and by their derivative, SB623 cells, supports neural cell growth. J. Neurosci. Res. 87(14):3198-3206; 2009.
2. Araujo, D. M.; Cotman, C. W. Trophic effects of interleukin-4, -7 and -8 on hippocampal neuronal cultures: Potential involvement of glial-derived factors. Brain Res. 600(1):49-55; 1993.
3. Arnhold, S.; Klein, H.; Klinz, F. J.; Absenger, Y.; Schmidt, A.; Schinkothe, T.; Brixius, K.; Kozlowski, J.; Desai, B.; Bloch, W.; Addicks, K. Human bone marrow stroma cells display certain neural characteristics and integrate in the subventricular compartment after injection into the liquor system. Eur. J. Cell Biol. 85(6):551-565; 2006.
4. Barone, F. C.; Feuerstein, G. Z. Inflammatory mediators and stroke: New opportunities for novel therapeutics. J. Cereb. Blood Flow Metab. 19(8):819-834; 1999.
5. Chen, X.; Li, Y.; Wang, L.; Katakowski, M.; Zhang, L.; Chen, J.; Xu, Y.; Gautam, S. C.; Chopp, M. Ischemic rat brain extracts induce human marrow stromal cell growth factor production. Neuropathology 22(4):275-279; 2002. (Pubitemid 36142758)
6. Chen, X. D.; Dusevich, V.; Feng, J. Q.; Manolagas, S. C.; Jilka, R. L. Extracellular matrix made by bone marrow cells facilitates expansion of marrow-derived mesenchymal progenitor cells and prevents their differentiation into osteoblasts. J. Bone Miner. Res. 22(12):1943-1956; 2007.
7. Dezawa, M.; Kanno, H.; Hoshino, M.; Cho, H.; Matsumoto, N.; Itokazu, Y.; Tajima, N.; Yamada, H.; Sawada, H.; Ishikawa, H.; Mimura, T.; Kitada, M.; Suzuki, Y.; Ide, C. Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. J. Clin. Invest. 113(12):1701-1710; 2004.
8. Goldberg, M. P.; Choi, D. W. Combined oxygen and glucose deprivation in cortical cell culture: Calcium-dependent and calcium-independent mechanisms of neuronal injury. J. Neurosci. 13(8):3510-3524; 1993.
9. Gregory, C. A.; Gunn, W. G.; Reyes, E.; Smolarz, A. J.; Munoz, J.; Spees, J. L.; Prockop, D. J. How wnt signaling affects bone repair by mesenchymal stem cells from the bone marrow. Ann. NY Acad. Sci. 1049:97-106; 2005.
10. Hayase, M.; Kitada, M.; Wakao, S.; Itokazu, Y.; Nozaki, K.; Hashimoto, N.; Takagi, Y.; Dezawa, M. Committed neural progenitor cells derived from genetically modified bone marrow stromal cells ameliorate deficits in a rat model of stroke. J. Cereb. Blood Flow Metab. 29(8):1409-1420; 2009.
11. Iantosca, M. R.; McPherson, C. E.; Ho, S. Y.; Maxwell, G. D. Bone morphogenetic proteins-2 and -4 attenuate apoptosis in a cerebellar primitive neuroectodermal tumor cell line. J. Neurosci. Res. 56(3):248-258; 1999.
12. Jin, K.; Sun, Y.; Xie, L.; Childs, J.; Mao, X. O.; Greenberg, D. A. Post-ischemic administration of heparin-binding epidermal growth factor-like growth factor (HB-EGF) reduces infarct size and modifies neurogenesis after focal cerebral ischemia in the rat. J. Cereb. Blood Flow Metab. 24(4):399-408; 2004.
13. Kinnaird, T.; Stabile, E.; Burnett, M. S.; Lee, C. W.; Barr, S.; Fuchs, S.; Epstein, S. E. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ. Res. 94(5):678-685; 2004.
14. Kopen, G. C.; Prockop, D. J.; Phinney, D. G. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc. Natl. Acad. Sci. USA 96(19):10711-10716; 1999.
15. Krabbe, C.; Zimmer, J.; Meyer, M. Neural transdifferentiation of mesenchymal stem cells - a critical review. APMIS 113(11-12):831-844; 2005. (Pubitemid 43934224)
16. Lee, H. J.; Kim, K. S.; Park, I. H.; Kim, S. U. Human neural stem cells over-expressing VEGF provide neuroprotection, angiogenesis and functional recovery in mouse stroke model. PLoS ONE 2(1):e156; 2007.
17. Loddick, S. A.; Turnbull, A. V.; Rothwell, N. J. Cerebral interleukin-6 is neuroprotective during permanent focal cerebral ischemia in the rat. J. Cereb. Blood Flow Metab. 18(2):176-179; 1998.
18. Lu, P.; Tuszynski, M. H. Can bone marrow-derived stem cells differentiate into functional neurons? Exp. Neurol. 193(2):273-278; 2005.
19. Malagelada, C.; Xifro, X.; Minano, A.; Sabria, J.; Rodriguez-Alvarez, J. Contribution of caspase-mediated apoptosis to the cell death caused by oxygen-glucose deprivation in cortical cell cultures. Neurobiol. Dis. 20(1):27-37; 2005.
20. Martinez-Sanchez, M.; Striggow, F.; Schroder, U. H.; Kahlert, S.; Reymann, K. G.; Reiser, G. Na(+) and Ca(2+) homeostasis pathways, cell death and protection after oxygen-glucose-deprivation in organotypic hippocampal slice cultures. Neuroscience 128(4):729-740; 2004.
21. Mason, I. J.; Fuller-Pace, F.; Smith, R.; Dickson, C. FGF-7 (keratinocyte growth factor) expression during mouse development suggests roles in myogenesis, forebrain regionalisation and epithelial-mesenchymal interactions. Mech. Dev. 45(1):15-30; 1994.
22. Mimura, T.; Dezawa, M.; Kanno, H.; Yamamoto, I. Behavioral and histological evaluation of a focal cerebral infarction rat model transplanted with neurons induced from bone marrow stromal cells. J. Neuropathol. Exp. Neurol. 64(12):1108-1117; 2005.
23. Mitani, A.; Yanase, H.; Sakai, K.; Wake, Y.; Kataoka, K. Origin of intracellular Ca2+ elevation induced by in vitro ischemia-like condition in hippocampal slices. Brain Res. 601(1-2):103-110; 1993.
24. Morganti-Kossmann, M. C.; Rancan, M.; Stahel, P. F.; Kossmann, T. Inflammatory response in acute traumatic brain injury: A double-edged sword. Curr. Opin. Crit. Care 8(2):101-105; 2002.
25. Munoz-Elias, G.; Marcus, A. J.; Coyne, T. M.; Woodbury, D.; Black, I. B. Adult bone marrow stromal cells in the embryonic brain: Engraftment, migration, differentiation, and long-term survival. J. Neurosci. 24(19):4585-4595; 2004.
26. Parr, A. M.; Tator, C. H.; Keating, A. Bone marrow-derived mesenchymal stromal cells for the repair of central nervous system injury. Bone Marrow Transplant. 40(7):609-619; 2007. (Pubitemid 47456475)
27. 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.; Polli, E. Induction of neurotrophin expression via human adult mesenchymal stem cells: Implication for cell therapy in neurodegenerative diseases. Cell Transplant. 16(1):41-55; 2007. (Pubitemid 46516657)
28. Potapova, I. A.; Gaudette, G. R.; Brink, P. R.; Robinson, R. B.; Rosen, M. R.; Cohen, I. S.; Doronin, S. V. Mesenchymal stem cells support migration, extracellular matrix invasion, proliferation, and survival of endothelial cells in vitro. Stem Cells 25(7):1761-1768; 2007.
29. Rosamond, W.; Flegal, K.; Furie, K.; Go, A.; Greenlund, K.; Haase, N.; Hailpern, S. M.; Ho, M.; Howard, V.; Kissela, B.; Kittner, S.; Lloyd-Jones, D.; McDermott, M.; Meigs, J.; Moy, C.; Nichol, G.; O'Donnell, C.; Roger, V.; Sorlie, P.; Steinberger, J.; Thom, T.; Wilson, M.; Hong, Y., for the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics - 2008 update: A report from the American Heart Association statistics committee and stroke statistics subcommittee. Circulation 117(4):e25-146; 2008.
30. Sakai, T.; Johnson, K. J.; Murozono, M.; Sakai, K.; Magnuson, M. A.; Wieloch, T.; Cronberg, T.; Isshiki, A.; Erickson, H. P.; Fassler, R. Plasma fibronectin supports neuronal survival and reduces brain injury following transient focal cerebral ischemia but is not essential for skin-wound healing and hemostasis. Nat. Med. 7(3):324-330.; 2001.
31. 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.; Sanberg, P. R. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp. Neurol. 164(2):247-256; 2000.
32. Sang, Q. X. Complex role of matrix metalloproteinases in angiogenesis. Cell Res. 8(3):171-177; 1998.
33. Shelton, D. N.; Chang, E.; Whittier, P. S.; Choi, D.; Funk, W. D. Microarray analysis of replicative senescence. Curr. Biol. 9(17):939-945; 1999.
34. Shimamura, M.; Sato, N.; Waguri, S.; Uchiyama, Y.; Hayashi, T.; Iida, H.; Nakamura, T.; Ogihara, T.; Kaneda, Y.; Morishita, R. Gene transfer of hepatocyte growth factor gene improves learning and memory in the chronic stage of cerebral infarction. Hypertension 47(4):742-751; 2006. (Pubitemid 43740247)
35. Taga, T.; Fukuda, S. Role of IL-6 in the neural stem cell differentiation. Clin. Rev. Allergy Immunol. 28(3):249-256; 2005.
36. Tang, Y.; Yasuhara, T.; Hara, K.; Matsukawa, N.; Maki, M.; Yu, G.; Xu, L.; Hess, D. C.; Borlongan, C. V. Transplantation of bone marrow-derived stem cells: A promising therapy for stroke. Cell Transplant. 16(2):159-169; 2007.
37. Tate, C. C.; Garcia, A. J.; LaPlaca, M. C. Plasma fibronectin is neuroprotective following traumatic brain injury. Exp. Neurol. 207(1):13-22; 2007.
38. Vana, A. C.; Flint, N. C.; Harwood, N. E.; Le, T. Q.; Fruttiger, M.; Armstrong, R. C. Platelet-derived growth factor promotes repair of chronically demyelinated white matter. J. Neuropathol. Exp. Neurol. 66(11):975-988; 2007.
39. Wang, L.; Li, Y.; Chen, X.; Chen, J.; Gautam, S. C.; Xu, Y.; Chopp, M. MCP-1, MIP-1, IL-8 and ischemic cerebral tissue enhance human bone marrow stromal cell migration in interface culture. Hematology 7(2):113-117; 2002.
40. Wang, M.; Crisostomo, P. R.; Herring, C.; Meldrum, K. K.; Meldrum, D. R. Human progenitor cells from bone marrow or adipose tissue produce VEGF, HGF, and IGF-I in response to TNF by a p38 MAPK-dependent mechanism. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291(4):R880-884; 2006.
41. Wang, Y. Q.; Guo, X.; Qiu, M. H.; Feng, X. Y.; Sun, F. Y. VEGF overexpression enhances striatal neurogenesis in brain of adult rat after a transient middle cerebral artery occlusion. J. Neurosci. Res. 85(1):73-82; 2007.
42. Yan, Y. P.; Sailor, K. A.; Lang, B. T.; Park, S. W.; Vemuganti, R.; Dempsey, R. J. Monocyte chemoattractant protein-1 plays a critical role in neuroblast migration after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 27(6):1213-1224; 2007.
43. Yasuhara, T.; Matsukawa, N.; Hara, K.; Maki, M.; Ali, M. M.; Yu, S.; Bae, E.; Yu, G.; Xu, L.; McGrogan, M.; Bankiewicz, K.; Case, C.; Borlongan, C. V. Notch-induced rat and human bone marrow stromal cell grafts reduce ischemic cell loss and ameliorate behavioral deficits in chronic stroke animals. Stem Cells Dev. 18(10):1501-1514; 2009.
44. Zhao, L. R.; Duan, W. M.; Reyes, M.; Keene, C. D.; Verfaillie, C. M.; Low, W. C. Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological deficits after grafting into the ischemic brain of rats. Exp. Neurol. 174(1):11-20; 2002.
45. Zhong, C.; Qin, Z.; Zhong, C. J.; Wang, Y.; Shen, X. Y. Neuroprotective effects of bone marrow stromal cells on rat organotypic hippocampal slice culture model of cerebral ischemia. Neurosci. Lett. 342(1-2):93-96; 2003.