Improvement of neurological deficits by intracerebral transplantation of human adipose tissue-derived stromal cells after cerebral ischemia in rats

Experimental Neurology

Volumn 183, Issue 2, 2003, Pages 355-366

  Kang, Soo Kyung ^a   Lee, Dong Hyung ^a   Bae, Yong Chan ^a   Kim, Hae Kyu ^a   Baik, Sun Yong ^a   Jung, Jin Sup ^a  

^a Pusan National University School of Medicine   (South Korea)

Author keywords

Adipose tissue stromal cells; BDNF; Brain ischemia; Transplantation

Indexed keywords

AZACITIDINE; GLIAL FIBRILLARY ACIDIC PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2;

ADENOVIRUS; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; BRAIN ISCHEMIA; CELL MIGRATION; CELL TRANSPLANTATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; INJECTION; LATERAL BRAIN VENTRICLE; LIPOSUCTION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; RAT; STATISTICAL SIGNIFICANCE; STROMA CELL;

EID: 0141449060     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4886(03)00089-X     Document Type: Article

References (54)

1. Ahmed S., Reynolds B.A., Weiss S. BDNF enhances the differentiation but not the survival of CNS stem cell-derived neuronal precursors. J. Neurosci. 15:1995;5765-5778.
2. Andsberg G., Kokaia Z., Klein R.L., Muzyczka N., Lindvall O., Mandel R.J. Neuropathological and behavioral consequences of adeno-associated viral vector-mediated continuous intrastriatal neurotrophin delivery in a focal ischemia model in rats. Neurobiol. Dis. 9:2002;187-204.
3. Azizi S.A., Stokes D., Augelli B.J., DiGirolamo C., Prockop D.J. Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats - similarities to astrocyte grafts. Proc. Natl. Acad. Sci. USA. 95:1998;3908-3913.
4. Barry F.P., Boynton R.E., Haynesworth S., Murphy J.M., Zaia M. The monoclonal antibody SH-2, raised against human mesenchymal stem cells, recognizes an epitope on endoglin (CD105). Biochem. Biophys. Res. Commun. 265:1999;134-139.
5. Beck T., Lindholm D., Castren E., Wree A. Brain-derived neurotrophic factor protects against ischemic cell damage in rat hippocampus. J. Cereb. Blood Flow Metab. 14:1994;689-692.
6. Bjorklund A. Neurobiology. Better cells for brain repair. Nature. 362:1993;414-415.
7. Bjorklund L.M., Sanchez-Pemaute R., Chung S., Andersson T., Chen I.Y., McNaught K.S., Brownell A.L., Jenkins B.G., Wahlestedt C., Kim K.S., Isacson O. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc. Natl. Acad. Sci. USA. 99:2002;2344-2349.
8. Brazelton T.R., Rossi F.M., Keshet G.I., Blau H.M. From marrow to brain expression of neuronal phenotypes in adult . Science. 290:2000;1775-1779.
9. Bruder S.P., Jaiswal N., Ricalton N.S., Mosca J.D., Kraus K.H., Kadiyala S. Mesenchymal stem cells in osteobiology and applied bone regeneration. Clin. Orthop. 355S:1998;S247-S256.
10. Cameron H.A., Hazel T.G., McKay R.D. Regulation of neurogenesis by growth factors and neurotransmitters. J. Neurobiol. 36:1998;287-306.
11. Campagnoli C., Roberts I.A., Kumar S., Bennett P.R., Bellantuono I., Fisk N.M. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood. 98:2001;2396-2402.
12. Chen H.M., Chopp Z., Zhang G., Garcia J.H. The effect of hypothermia on transient middle cerebral artery occlusion in the rat. J. Cereb. Blood Flow Metab. 12:1992;621-628.
13. Chen J., Li Y., Chopp M. Intracerebral transplantation of bone marrow with BDNF after MCAo in rat. Neuropharmacology. 39:2000;711-716.
14. Chen Y., Constantini S., Trembovler V., Weinstock M., Shohami E. An experimental model of closed head injury in mice pathophysiology, histopathology, and cognitive deficits . J. Neurotrauma. 13:1996;557-568.
15. Defer G.L., Geny C., Ricolfi F., Fenelon G., Monfort J.C., Remy P., Villafane G., Jeny R., Samson Y., Keravel Y., Gaston A., Degos J.D., Peschanski M., Cesaro P., Nguyen J.P. Long-term outcome of unilaterally transplanted parkinsonian patients. I. Clinical approach. Brain. 119:1996;41-50.
16. Deng W., Obrocka M., Fischer I., Prockop D.J. In vitro differentiation of human marrow stromal cells into early progenitors of neural cells by conditions that increase intracellular cyclic AMP. Biochem. Biophys. Res. Commun. 282:2001;148-152.
17. Ding, L., Lu, S., Batchu, R., R. III, S., Munshi, N., 1999. Bone marrow stromal cells as a vehicle for gene transfer. Gene Ther. 6, 1611-1616.
18. Erickson G.R., Gimble J.M., Franklin D.M., Rice H.E., Awad H., Guilak F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem. Biophys. Res. Commun. 290:2002;763-769.
19. Gronthos S., Franklin D.M., Leddy H.A., Robey P.G., Storms R.W., Gimble J.M. Surface protein characterization of human adipose tissue-derived stromal cells. J. Cell Physiol. 189:2001;54-63.
20. Guillin O., Diaz J., Carrol I.P., Griffon N., Schwartz J.C., Sokoloff P. BDNF controls dopamine D3 receptor expression and triggers behavioural sensitization. Nature. 411:2001;86-89.
21. Halvorsen Y.D., Franklin D., Bond A.L., Hitt D.C., Auchter C., Boskey A.L., Paschalis E.P., Wilkison W.O., Gimble J.M. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng. 7:2001;729-741.
22. Hausman G.J., Campion D.R. Histology of the stroma in developing rat subcutaneous adipose tissue. J. Anim. Sci. 55:1982;1336-1342.
23. Hernandez T.D., Schallert T. Seizures and recovery from experimental brain damage. Exp. Neurol. 102:1988;318-324.
24. Jin H.K., Carter J.E., Huntley G.W., Schuchman E.H. Intracerebral transplantation of mesenchymal stem cells into acid sphingomyelinase-deficient mice delays the onset of neurological abnormalities and extends their life span. J. Clin. Invest. 109:2002;1183-1191.
25. Kang S.K., Lee R.H., Jung J.S. Effect of Brain-derived neurotrophic factor on neural differentiation of mouse embryonic stem cells and neural precursor cells. Neurosci. Res. Commun. 29:2001;183-192.
26. 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. 19:1999;10711-10716.
27. Li Y., Chopp M., Chen J., Wang L., Gautam S.C., Xu Y.X., Zhang Z.G. Intrastriatal transplantation of bone marrow nonhematopoietic cells improves functional recovery after stroke in adult mice. J. Cereb. Blood Flow Metab. 20:2000;1311-1319.
28. McDonald J.W., Liu X.Z., Qu Y., Liu S., Mickey S.K., Turetsky D., Gottlieb D.I., Choi D.W. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nature Med. 5:1999;1410-1412.
29. McKay R. Stem cells in the central nervous system. Science. 276:1997;66-71.
30. Mezey E., Chandross K.J., Harta G., Maki R.A., McKerche S.R. Turning blood into brain cells bearing neuronal antigens generated in vivo from bone marrow . Science. 290:2000;1779-1782.
31. Park K.W., Eglitis M.A., Mouradian M.M. Protection of nigral neurons by GDNF-engineered marrow cell transplantation. Neurosci. Res. 40:2001;315-323.
32. Patrick C.W. Adipose tissue engineering the future of breast and soft tissue reconstruction following tumor resection . Semin. Surg. Oncol. 19:2000;302-311.
33. Pereira R.F., Halford K.W., O'Hara M.D., Leeper D.B., Sokolov B.P., Pollard M.D., Bagasra O., Prockop D.J. Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc. Natl. Acad. Sci. USA. 92:1995;4857-4861.
34. Perez-Navarro E., Canudas A.M., Akerund P., Alberch J., Arenas E. Brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4/5 prevent the death of striatal projection neurons in a rodent model of Huntington's disease. J. Neurochem. 75:2000;2190-2199.
35. Pettersson P., Cigolini M., Sjoestroem L., Smith U., Bjoerntorp P. Cells in human adipose tissue developing into adipocytes. Acta Med. Scand. 215:1984;447-451.
36. Pittenger M.F., McKay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., Moorman M.A., Simonetti D.W., Craig S., Marshak D.R. Multilineage potential of adult human mesenchymal stem cells. Science. 284:1999;143-147.
37. Prockop D.J. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 276:1997;71-74.
38. Reyes M., Lund T., Lenvik T., Aguiar D., Koodie L., Verfaillie C.M. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood. 98:2001;2615-2625.
39. Safford K.M., Hicok K.C., Safford S.D., Halvorsen Y.D., Wilkison W.O., Gimble J.M., Rice H.E. Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem. Biophys. Res. Commun. 294:2002;371-379.
40. 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. 164:2000;247-256.
41. Schabitz W.R., Schwab S., Spranger M., Hacke W. Intraventricular brain-derived neurotrophic factor reduces infarct size after focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 17:1997;500-506.
42. Schallert T., Hernandez T.D., Barth T.M. Recovery of function after brain damage severe and chronic disruption by diazepam . Brain Res. 379:1986;104-111.
43. Suzuki K., Oyama M., Faulcon L., Robbins P.D., Niyibizi C. In vivo expression of human growth hormone by genetically modified murine bone marrow stromal cells and its effect on the cells in vitro. Cell Transplant. 9:2000;319-327.
44. Terada N., Hamazaki T., Oka M., Hoki M., Mastalerz D.M., Nakano Y., Meyer E.M., Morel L., Petersen B.E., Scott E.W. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature. 416:2002;542-545.
45. Tremain N., Korkko J., Ibberson D., Kopen G.C., DiGirolamo C., Phinney D.G. MicroSAGE analysis of 2,353 expressed genes in a single cell-derived colony of undifferentiated human mesenchymal stem cells reveals mRNAs of multiple cell lineages. Stem Cells. 19:2001;408-418.
46. Tucker K.L., Meyer M., Barde Y.A. Neurotrophins are required for nerve growth during development. Nat. Neurosci. 4:2001;29-37.
47. Turner D.A., Kearney W. Scientific and ethical concerns in neural fetal tissue transplantation. Neurosurgery. 33:1993;1031-1037.
48. Van Obberghen E., Kamholz J., Bishop J.G. III, Zomzely-Neurath C., Lazzarini R.A. Human gamma enolase isolation of a cDNA clone and expression in normal and tumor tissues of human origin . J. Neurosci. Res. 19:1988;450-456.
49. Weissman I.L. Translating stem and progenitor cell biology to the clinic barriers and opportunities . Science. 287:2000;1442-1446.
50. Wernig M., Brustle O. Fifty ways to make a neuron shifts in stem cell hierarchy and their implications for neuropathology and CNS repair . J. Neuropathol. Exp. Neurol. 61:2002;101-110.
51. Woodbury D., Schwarz E.J., Prockop D.J., Black I.B. Adult rat and human bone marrow stromal cells differentiate into neurons. J. Neurosci. Res. 61:2000;364-370.
52. Ying Q.L., Nichols J., Evans E.P., Smith A.G. Changing potency by spontaneous fusion. Nature. 416:2002;545-548.
53. Zhao L.R., Duan W.M., Reyes M., eene 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. 174:2002;11-20.
54. Zuk P.A., Zuh M., Mizuno H., Huang J., Futrell J.W., Katz A.J., Benhaim P., Lorenz H.P., Hedrick M.H. Multilineage cells from human adipose tissue implications for cell-based therapies . Tissue Eng. 7:2001;209-226.