Transplanted Hematopoietic Stem Cells from Bone Marrow Differentiate into Neural Lineage Cells and Promote Functional Recovery after Spinal Cord Injury in Mice

Journal of Neuropathology and Experimental Neurology

Volumn 63, Issue 1, 2004, Pages 64-72

  Koshizuka, Shuhei ^a   Okada, Seiji ^b   Okawa, Akihiko ^a   Koda, Masao ^a   Murasawa, Mitsuhiro ^a   Hashimoto, Masayuki ^a   Kamada, Takahito ^a   Yoshinaga, Katsunori ^a,c   Murakami, Masazumi ^a   Moriya, Hideshige ^a   Yamazaki, Masashi ^a  

^a CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

^c CHIBA UNIVERSITY HOSPITAL   (Japan)

Author keywords

Bone marrow; Hematopoietic stem cell; Spinal cord injury; Transplantation

Indexed keywords

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL LINEAGE; CELL REGENERATION; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GRAFT SURVIVAL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HINDLIMB; IMMUNOHISTOCHEMISTRY; MOTOR PERFORMANCE; MOUSE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; REMYELINIZATION; SPINAL CORD INJURY; Y CHROMOSOME;

EID: 9144273814     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1093/jnen/63.1.64     Document Type: Article

References (39)

1. Schwab ME, Bartholdi D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev 1996;76:319-70
2. Bracken MB. Methylprednisolone and acute spinal cord injury: An update of the randomized evidence. Spine 2001;26:S47-54
3. Gussoni E, Soneoka Y, Strickland CD, et al. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 1999;401:390-94
4. Lagasse E, Connors H, Al-Dhalimy M, et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 2000;6:1229-34
5. Orlic D, Kajstura J, Chimenti S, et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001;410:701-5
6. Brazelton TR, Rossi FM, Keshet GI, et al. From marrow to brain: Expression of neuronal phenotypes in adult mice. Science 2000;290:1775-79
7. Eglitis MA, Mezey E. Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc Natl Acad Sci U S A 1997;94:4080-85
8. Mezey E, Chandross KJ, Harta G, et al. Turning blood into brain: Cells bearing neuronal antigens generated in vivo from bone marrow. Science 2000;290:1779-82
9. Okada S, Nakauchi H, Nagayoshi K, et al. In vivo and in vitro stem cell function of c-kit- and Sca-1-positive murine hematopoietic cells. Blood 1992;80:3044-50
10. Uchida N, Weissman IL. Searching for hematopoietic stem cells: Evidence that Thy-1.1lo Lin- Sca-1 + cells are the only stem cells in C57BL/Ka-Thy-1.1 bone marrow. J Exp Med 1992;175:175-84
11. Kondo M, Wagers AJ, Manz MG, et al. Biology of hematopoietic stem cells and progenitors: Implications for clinical application. Ann Rev Immunol 2003;21:759-806
12. Okada S, Yoshida T, Honq Z, et al. Impairment of B lymphopoiesis in precocious aging (klotho) mice. Int Immunol 2000;12:861-71
13. Farooque M. Spinal cord compression injury in the mouse: Presentation of a model including assessment of motor dysfunction. Acta Neuropathol 2000;100:13-22
14. Zambrowicz BP, Imamoto A, Fiering S, et al. Disruption of overlapping transcripts in the ROSA beta geo 26 gene trap strain leads to widespread expression of beta-galactosidase in mouse embryos and hematopoietic cells. Proc Natl Acad Sci U S A 1997;94:3789-94
15. Widner H, Brundin P. Immunological aspects of grafting in the mammalian central nervous system. A review and speculative synthesis. Brain Res 1988;472:287-324
16. Basso DM, Beattie MS, Bresnahan JC. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 1995;12:1-21
17. Hashimoto M, Koda M, Ino H, Murakami M, Yamazaki M, Moriya H. Upregulation of osteopontin expression in rat spinal cord microglia after traumatic injury. J Neurotrauma 2003;20:287-96
18. Darzynkiewicz Z, Traganos F, Kapuscinski J, Staiano-Coico L, Melamed MR. Accessibility of DNA in situ to various fluorochromes: Relationship to chromatin changes during erythroid differentiation of Friend leukemia cells. Cytometry 1984;5:355-63
19. Corti S, Locatelli F, Donadoni C, et al. Neuroectodermal and microglial differentiation of bone marrow cells in the mouse spinal cord and sensory ganglia. J Neurosci Res 2002;70:721-33
20. Truong K, Vielh P, Malfoy B, et al. Fluorescence-based analysis of DNA ploidy and cell proliferation within fine-needle samplings of breast tumors: A new approach using automated image cytometry. Cancer 1998;84:309-16
21. Chen J, Li Y, Wang L, Lu M, Zhang X, Chopp M. Therapeutic benefit of intracerebral transplantation of bone marrow stromal cells after cerebral ischemia in rats. J Neurol Sci 2001;189:49-57
22. Chopp M, Zhang XH, Li Y, et al. Spinal cord injury in rat: Treatment with bone marrow stromal cell transplantation. Neuroreport 2000;11:3001-5
23. Nakano K, Migita M, Mochizuki H, Shimada T Differentiation of transplanted bone marrow cells in the adult mouse brain. Transplantation 2001;71:1735-40
24. Jiang Y, Jahagirdar BN, Reinhardt RL, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002;418:41-49
25. Huss R. Perspectives on the morphology and biology of CD34-negative stem cells. J Hematother Stem Cell Res 2000;9:783-93
26. Cao QL, Zhang YP, Howard RM, Walters WM, Tsoulfas P, Whittemore SR. Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Exp Neurol 2001;167:48-58
27. Cao QL, Howard RM, Dennison JB, Whittemore SR. Differentiation of engrafted neuronal-restricted precursor cells is inhibited in the traumatically injured spinal cord. Exp Neurol 2002;177:349-59
28. Yamamoto S, Yamamoto N, Kitamura T, Nakamura K, Nakafuku M. Proliferation of parenchymal neural progenitors in response to injury in the adult rat spinal cord. Exp Neurol 2001;172:115-27
29. Shihabuddin LS, Horner PJ, Ray J, Gage FH. Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J Neurosci 2000;20:8727-35
30. Wagers AJ, Sherwood RI, Christensen JL, Weissman IL. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 2002;297:2256-59
31. Wurmser AE, Gage FH. Stem cells: Cell fusion causes confusion. Nature 2002;416:485-87
32. Terada N, Hamazaki T, Oka M, et al. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 2002;416:542-45
33. Ying QL, Nichols J, Evans EP, Smith AG. Changing potency by spontaneous fusion. Nature 2002;416:545-48
34. Shibuya S, Miyamoto O, Itano T, Mori S, Norimatsu H. Temporal progressive antigen expression in radial glia after contusive spinal cord injury in adult rats. Glia 2003;42:172-83
35. Takahashi M, Arai Y, Kurosawa H, et al. Ependymal cell reactions in spinal cord segments after compression injury in adult rat. J Neuropathol Exp Neurol 2003;62:185-94
36. Takakura N, Watanabe T, Suenobu S, et al. A role for hematopoietic stem cells in promoting angiogenesis. Cell 2000;102:199-209
37. Valable S, Bellail A, Lesne S, et al. Angiopoietin-1-induced PI3-kinase activation prevents neuronal apoptosis. FASEB J 2003;17:443-45
38. Zhang ZG, Zhang L, Croll SD, Chopp M. Angiopoietin-1-reduces cerebral blood vessel leakage and ischemic lesion volume after focal cerebral embolic ischemia in mice. Neuroscience 2002;113:683-87
39. Ogawa Y, Sawamoto K, Miyata T, et al. Transplantation of in vitro-expanded fetal neural progenitor cells results in neurogenesis and functional recovery after spinal cord contusion injury in adult rats. J Neurosci Res 2002;69:925-33