Transplanted bone marrow stem cells relocate to infarct penumbra and co-express endogenous proliferative and immature neuronal markers in a mouse model of ischemic cerebral stroke

BMC Neuroscience

Volumn 11, Issue , 2010, Pages

  Zhang, Xue Mei ^a   Du, Fang ^a   Yang, Dan ^a   Yu, Chun Jiang ^a   Huang, Xiang Nan ^a   Liu, Wei ^a   Fu, Jin ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CYCLINE; DOUBLECORTIN; DOUBLECORTIN PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NEUROPEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; BRAIN CORTEX; BRAIN INFARCTION; BRAIN ISCHEMIA; CELL PROLIFERATION; CONTROLLED STUDY; CYTOFLUOROMETRY; EXPERIMENTAL MODEL; FLUORESCENCE ACTIVATED CELL SORTING; FOREBRAIN; IMMUNOHISTOCHEMISTRY; INTERNEURON; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN LOCALIZATION; STEM CELL TRANSPLANTATION; STROKE; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; FEMALE; FLOW CYTOMETRY; GENETICS; MALE; METABOLISM; NERVE REGENERATION; PHYSIOLOGY;

ANIMALS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; BRAIN ISCHEMIA; CELL PROLIFERATION; CEREBRAL INFARCTION; FEMALE; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED BALB C; MICROTUBULE-ASSOCIATED PROTEINS; NERVE REGENERATION; NEURONS; NEUROPEPTIDES; PROLIFERATING CELL NUCLEAR ANTIGEN; STROKE;

EID: 77958138738     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-11-138     Document Type: Article

References (42)

1. Zhang ZG, Zhang L, Jiang Q, Chopp M. Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse. Circ Res 2002, 90:284-288. 10.1161/hh0302.104460, 11861416.
2. Fotheringham AP, Davies CA, Davies I. Oedema and glial cell involvement in the aged mouse brain after permanent focal ischaemia. Neuropathol Appl Neurobiol 2000, 26:412-423. 10.1046/j.1365-2990.2000.00265.x, 11054181.
3. Xiong Y, Mahmood A, Chopp M. Angiogenesis, neurogenesis and brain recovery of function following injury. Curr Opin Investig Drugs 2010, 11:298-308.
4. Magavi SS, Macklis JD. Induction of neuronal type-specific neurogenesis in the cerebral cortex of adult mice: manipulation of neural precursors in situ. Brain Res Dev Brain Res 2002, 134:57-76. 10.1016/S0165-3806(01)00316-9, 11947937.
5. Arlotta P, Magavi SS, Macklis JD. Molecular manipulation of neural precursors in situ: induction of adult cortical neurogenesis. Exp Gerontol 2003, 38:173-182. 10.1016/S0531-5565(02)00156-0, 12543275.
6. Jin K, Wang X, Xie L, Mao XO, Zhu W, Wang Y, Shen J, Mao Y, Banwait S, Greenberg DA. Evidence for stroke-induced neurogenesis in the human brain. Proc Natl Acad Sci USA 2006, 103:13198-13202. 10.1073/pnas.0603512103, 1559776, 16924107.
7. Gould E. How widespread is adult neurogenesis in mammals?. Nature reviews. Neurosci 2007, 8:481-488.
8. Gross CG. Neurogenesis in the adult brain: death of a dogma. Nature reviews. Neurosci 2000, 1:67-73.
9. Zhao C, Deng W, Gage FH. Mechanisms and functional implications of adult neurogenesis. Cell 2008, 132:645-660. 10.1016/j.cell.2008.01.033, 18295581.
10. Mattiesen WR, Tauber SC, Gerber J, Bunkowski S, Bruck W, Nau R. Increased neurogenesis after hypoxic-ischemic encephalopathy in humans is age related. Acta Neuropathol 2009, 117:525-534. 10.1007/s00401-009-0509-0, 19277687.
11. Shen CC, Yang YC, Chiao MT, Cheng WY, Tsuei YS, Ko JL. Characterization of endogenous neural progenitor cells after experimental ischemic stroke. Curr Neurovasc Res 2010, 7:6-14. 10.2174/156720210790820208, 20158467.
12. Urrea C, Castellanos DA, Sagen J, Tsoulfas P, Bramlett HM, Dietrich WD. Widespread cellular proliferation and focal neurogenesis after traumatic brain injury in the rat. Restor Neurol Neurosci 2007, 25:65-76.
13. Wang Y, Jin K, Greenberg DA. Neurogenesis associated with endothelin-induced cortical infarction in the mouse. Brain Res 2007, 1167:118-122. 10.1016/j.brainres.2007.06.065, 2098871, 17669376.
14. Gu W, Gu C, Jiang W, Wester P. Neurotransmitter synthesis in poststroke cortical neurogenesis in adult rats. Stem Cell Res 2010, 4:148-154. 10.1016/j.scr.2009.12.001, 20089468.
15. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002, 418:41-49. 10.1038/nature00870, 12077603.
16. Atala A, Koh CJ. Tissue engineering applications of therapeutic cloning. Annu Rev Biomed Eng 2004, 6:27-40. 10.1146/annurev.bioeng.6.012204.115707, 15255761.
17. Grove JE, Bruscia E, Krause DS. Plasticity of bone marrow-derived stem cells. Stem Cells 2004, 22:487-500. 10.1634/stemcells.22-4-487, 15277695.
18. Mezey E, Chandross KJ, Harta G, Maki RA, McKercher SR. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 2000, 290:1779-1782. 10.1126/science.290.5497.1779, 11099419.
19. Cogle CR, Yachnis AT, Laywell ED, Zander DS, Wingard JR, Steindler DA, Scott EW. Bone marrow transdifferentiation in brain after transplantation: a retrospective study. Lancet 2004, 363:1432-1437. 10.1016/S0140-6736(04)16102-3, 15121406.
20. Hess DC, Hill WD, Martin-Studdard A, Carothers J, Brailer J, Carroll J. Blood into brain after stroke. Trends Mol Med 2002, 8:452-453. 10.1016/S1471-4914(02)02404-8, 12223318.
21. Ji KH, Xiong J, Fan LX, Hu KM, Liu HQ. Rat marrow-derived multipotent adult progenitor cells differentiate into skin epidermal cells in vivo. J Dermatol 2009, 36:403-409. 10.1111/j.1346-8138.2009.00666.x, 19583688.
22. Zhang XM, Cai Y, Chu Y, Chen EY, Feng JC, Luo XG, Xiong K, Struble RG, Clough RW, Patrylo PR, Kordower JH, Yan XX. Doublecortin-expressing cells persist in the associative cerebral cortex and amygdala in aged nonhuman primates. Front Neuroanat 2009, 3:17. 10.3389/neuro.05.017.2009, 2766270, 19862344.
23. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 2003, 467:1-10. 10.1002/cne.10874, 14574675.
24. Okada S, Nakauchi H, Nagayoshi K, Nishikawa S, Miura Y, Suda T. In vivo and in vitro stem cell function of c-kit- and Sca-1-positive murine hematopoietic cells. Blood 1992, 80:3044-3050.
25. Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Silva GV, Mesquita CT, Belem L, Vaughn WK, Rangel FO, Assad JA, Carvalho AC, Branco RV, Rossi MI, Dohmann HJ, Willerson JT. Improved exercise capacity and ischemia 6 and 12 months after transendocardial injection of autologous bone marrow mononuclear cells for ischemic cardiomyopathy. Circulation 2004, 110:II213-218. 10.1161/01.CIR.0000138398.77550.62, 15364865.
26. Wollert KC, Meyer GP, Lotz J, Ringes-Lichtenberg S, Lippolt P, Breidenbach C, Fichtner S, Korte T, Hornig B, Messinger D, Arseniev L, Hertenstein B, Ganser A, Drexler H. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet 2004, 364:141-148. 10.1016/S0140-6736(04)16626-9, 15246726.
27. Koh LP, Hwang WY, Tan CH, Linn YC, Goh YT, Chuah CT, Ng HJ, Fook-Chong SM, Tan PH. Long term follow-up of Asian patients with chronic myeloid leukemia (CML) receiving allogeneic hematopoietic stem cell transplantation (HSCT) from HLA-identical sibling-evaluation of risks and benefits. Ann Hematol 2004, 83:286-294. 10.1007/s00277-003-0810-2, 15060748.
28. Borlongan CV. Cell therapy for stroke: remaining issues to address before embarking on clinical trials. Stroke 2009, 40:S146-148. 10.1161/STROKEAHA.108.533091, 19064801.
29. Ohta T, Kikuta K, Imamura H, Takagi Y, Nishimura M, Arakawa Y, Hashimoto N, Nozaki K. Administration of ex vivo-expanded bone marrow-derived endothelial progenitor cells attenuates focal cerebral ischemia-reperfusion injury in rats. Neurosurgery 2006, 59:679-686. 10.1227/01.NEU.0000229058.08706.88, 16955050.
30. Tomita T, Takeuchi E, Toyosaki-Maeda T, Oku H, Kaneko M, Takano H, Sugamoto K, Ohzono K, Suzuki R, Ochi T. Establishment of nurse-like stromal cells from bone marrow of patients with rheumatoid arthritis: indication of characteristic bone marrow microenvironment in patients with rheumatoid arthritis. Rheumatology (Oxford) 1999, 38:854-863. 10.1093/rheumatology/38.9.854, 10515647.
31. Yau TM, Tomita S, Weisel RD, Jia ZQ, Tumiati LC, Mickle DA, Li RK. Beneficial effect of autologous cell transplantation on infarcted heart function: comparison between bone marrow stromal cells and heart cells. Ann Thorac Surg 2003, 75:169-176. discussion 176-177., 10.1016/S0003-4975(02)04290-X, 12537212.
32. Strauer BE, Brehm M, Zeus T, Kostering M, Hernandez A, Sorg RV, Kogler G, Wernet P. Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation 2002, 106:1913-1918. 10.1161/01.CIR.0000034046.87607.1C, 12370212.
33. Terai S, Sakaida I, Yamamoto N, Omori K, Watanabe T, Ohata S, Katada T, Miyamoto K, Shinoda K, Nishina H, Okita K. An in vivo model for monitoring trans-differentiation of bone marrow cells into functional hepatocytes. J Biochem 2003, 134:551-558. 10.1093/jb/mvg173, 14607982.
34. Jin SZ, Meng XW, Han MZ, Sun X, Sun LY, Liu BR. Stromal cell derived factor-1 enhances bone marrow mononuclear cell migration in mice with acute liver failure. World J Gastroenterol 2009, 15:2657-2664. 10.3748/wjg.15.2657, 2691499, 19496198.
35. Chen J, Li Y, Wang L, Zhang Z, Lu D, Lu M, Chopp M. Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 2001, 32:1005-1011.
36. Lu D, Mahmood A, Wang L, Li Y, Lu M, Chopp M. Adult bone marrow stromal cells administered intravenously to rats after traumatic brain injury migrate into brain and improve neurological outcome. Neuroreport 2001, 12:559-563. 10.1097/00001756-200103050-00025, 11234763.
37. Chopp M, Li Y. Treatment of neural injury with marrow stromal cells. Lancet Neurol 2002, 1:92-100. 10.1016/S1474-4422(02)00040-6, 12849513.
38. Crain BJ, Tran SD, Mezey E. Transplanted human bone marrow cells generate new brain cells. J Neurol Sci 2005, 233:121-123. 10.1016/j.jns.2005.03.017, 15949500.
39. Kawada H, Takizawa S, Takanashi T, Morita Y, Fujita J, Fukuda K, Takagi S, Okano H, Ando K, Hotta T. Administration of hematopoietic cytokines in the subacute phase after cerebral infarction is effective for functional recovery facilitating proliferation of intrinsic neural stem/progenitor cells and transition of bone marrow-derived neuronal cells. Circulation 2006, 113:701-710. 10.1161/CIRCULATIONAHA.105.563668, 16461843.
40. Hess DC, Hill WD, Martin-Studdard A, Carroll J, Brailer J, Carothers J. Bone marrow as a source of endothelial cells and NeuN-expressing cells After stroke. Stroke 2002, 33:1362-1368. 10.1161/01.STR.0000014925.09415.C3, 11988616.
41. Nadri S, Soleimani M, Hosseni RH, Massumi M, Atashi A, Izadpanah R. An efficient method for isolation of murine bone marrow mesenchymal stem cells. Int J Dev Biol 2007, 51:723-729. 10.1387/ijdb.072352ns, 17939119.
42. Jin SZ, Meng XW, Sun X, Han MZ, Liu BR, Wang XH, Sun LY, Huang Q, Zhao RB, Ban X, Yu HY, Yu HW. Granulocyte Colony-Stimulating Factor Enhances Bone Marrow Mononuclear Cell Homing to the Liver in a Mouse Model of Acute Hepatic Injury. Dig Dis Sci 2010,