Repetitive intrathecal catheter delivery of bone marrow mesenchymal stromal cells improves functional recovery in a rat model of contusive spinal cord injury

Journal of Neurotrauma

Volumn 28, Issue 9, 2011, Pages 1951-1961

  Cizkova, Dasa ^a   Novotna, Ivana ^a   Slovinska, Lucia ^a   Vanicky, Ivo ^a   Jergova, Stanislava ^b   Rosocha, Jan ^c   Radonak, Jozef ^c  

^a INSTITUTE OF CHEMISTRY   (Slovakia)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c P J AFÁRIK UNIVERSITY   (Slovakia)

Author keywords

neuroplasticity; regeneration; stem cells; traumatic spinal cord injury

Indexed keywords

STROMAL CELL DERIVED FACTOR 1;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY; ARTICLE; BONE MARROW; BONE MARROW TRANSPLANTATION; BRAIN DAMAGE; CATHETER; CATHETERIZATION; CELL CULTURE; CELL SURVIVAL; CELL TRANSPLANTATION; CONTROLLED STUDY; CONTUSION; ENGRAFTMENT; HISTOPATHOLOGY; LOCOMOTION; MESENCHYMAL STEM CELL TRANSPLANTATION; MOTOR PERFORMANCE; NONHUMAN; PIA MATER; RAT; RATING SCALE; SPINAL CORD INJURY; WHITE MATTER;

ANIMALS; BONE MARROW TRANSPLANTATION; MALE; MESENCHYMAL STROMAL CELLS; MOTOR ACTIVITY; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; SPINAL CORD INJURIES;

EID: 80054797887     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2010.1413     Document Type: Article

References (53)

1. Allen, J.W., Horais, K.A., Tozier, N.A., Wegner, K., Corbeil, J.A., Mattrey, R.F., Rossi, S.S., and Yaksh, T.L. (2006). Time course and role of morphine dose and concentration in intrathecal granuloma formation in dogs: A combined magnetic resonance imaging and histopathology investigation. Anesthesiology 105, 581-589.
2. Bai, H., Suzuki, Y., Noda, T., Wu, S., Kataoka, K., Kitada, M., Ohta, M., Chou, H., and Ide, C. (2003). Dissemination and proliferation of neural stem cells on the spinal cord by injection into the fourth ventricle of the rat: A method for cell transplantation. J. Neurosci. Methods 124, 181-187.
3. Basso, D.M., Beattie, M.S., and Bresnahan, J.C. (1995). A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 12, 1-21.
4. Berrocal, Y., Pearse, D.D., Singh, A., Andrade, C.M., McBroom, J.S., Puentes, R., and Eaton, M.J. (2007). Social and environmental enrichment improves sensory and motor recovery after severe contusive spinal cord injury in the rat. J. Neurotrauma 24, 1761-1772.
5. Butler, J.M., Nolan, D.J., Vertes, E.L., Varnum-Finney, B., Kobayashi, H., Hooper, A.T., Seandel, M., Shido, K., White, I.A., Kobayashi, M., Witte, L., May, C., Shawber, C., Kimura, Y., Kitajewski, J., Rosenwaks, Z., Bernstein, I.D., and Rafii, S. (2010). Endothelial cells are essential for the self-renewal and repopulation of Notch-dependent hematopoietic stem cells. Cell Stem Cell 6, 251-264.
6. Cizkova, D., Kakinohana, O., Kucharova, K., Marsala, S., Johe, K., Hazel, T., Hefferan, M.P., and Marsala, M. (2007). Functional recovery in rats with ischemic paraplegia after spinal grafting of human spinal stem cells. Neuroscience 147, 546-560.
7. Cizkova, D., Nagyova, M., Slovinska, L., Novotna, I., Radonak, J., Cizek, M., Mechirova, E., Tomori, Z., Hlucilova, J., Motlik, J., Sulla, I., Jr., and Vanicky, I. (2009). Response of ependymal progenitors to spinal cord injury or enhanced physical activity in adult rat. Cell. Mol. Neurobiol. 29, 999-1013.
8. Cizkova, D., Rosocha, J., Vanicky, I., Jergova, S., and Cizek, M. (2006a). Transplants of human mesenchymal stem cells improve functional recovery after spinal cord injury in the rat. Cell Mol. Neurobiol. 26, 1165-1178.
9. Cizkova, D., Rosocha, J., Vanicky, I., Radonak, J., Galik, J., and Cizek, M. (2006b). Induction of mesenchymal stem cells leads to HSP72 synthesis and higher resistance to oxidative stress. Neurochem. Res. 31, 1011-1020.
10. Conrad, S., Renninger, M., Hennenlotter, J., Wiesner, T., Just, L., Bonin, M., Aicher, W., Buhring, H.J., Mattheus, U., Mack, A., Wagner, H.J., Minger, S., Matzkies, M., Reppel, M., Hescheler, J., Sievert, K.D., Stenzl, A., and Skutella, T. (2008). Generation of pluripotent stem cells from adult human testis. Nature 456, 344-349.
11. Coutts, M., and Keirstead, H.S. (2008). Stem cells for the treatment of spinal cord injury. Exp. Neurol. 209, 368-377.
12. Crowe, M.J., Bresnahan, J.C., Shuman, S.L., Masters, J.N., and Beattie, M.S. (1997). Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat. Med. 3, 73-76.
13. Djouad, F., Plence, P., Bony, C., Tropel, P., Apparailly, F., Sany, J., Noel, D., and Jorgensen, C. (2003). Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 102, 3837-3844.
14. Eaton, M.J., Pearse, D.D., McBroom, J.S., and Berrocal, Y.A. (2008). The combination of human neuronal serotonergic cell implants and environmental enrichment after contusive SCI improves motor recovery over each individual strategy. Behav. Brain Res. 194, 236-241.
15. Elisseeff, J.H. (2004). Embryonic stem cells: Potential for more impact. Trends Biotechnol. 22, 155-156.
16. Fawcett, J.W., and Asher, R.A. (1999). The glial scar and central nervous system repair. Brain Res. Bull. 49, 377-391.
17. Garbuzova-Davis, S., and Sanberg, P.R. (2009). Feasibility of cell therapy for amyotrophic lateral sclerosis. Exp. Neurol. 216, 3-6.
18. Greco, S.J., and Rameshwar, P. (2008). Microenvironmental considerations in the application of human mesenchymal stem cells in regenerative therapies. Biologics 2, 699-705.
19. Hassenbusch, S., Burchiel, K., Coffey, R.J., Cousins, M.J., Deer, T., Hahn, M.B., Pen, S.D., Follett, K.A., Krames, E., Rogers, J.N., Sagher, O., Staats, P.S., Wallace, M., and Willis, K.D. (2002). Management of intrathecal catheter-tip inflammatory masses: A consensus statement. Pain Med. 3, 313-323.
20. Hayes, C.S., Mulkmus, S.A., Cizkova, D., Yaksh, T.L., and Hua, X.Y. (2003). A double-lumen intrathecal catheter for studies of modulation of spinal opiate tolerance. J. Neurosci. Methods 126, 165-173.
21. Hebl, J.R. (2008). Ultrasound-guided regional anesthesia and the prevention of neurologic injury: Fact or fiction? Anesthesiology 108, 186-188.
22. Hofstetter, C.P., Schwarz, E.J., Hess, D., Widenfalk, J., El Manira, A., Prockop, D.J., and Olson, L. (2002). Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc. Natl. Acad. Sci. USA 99, 2199-2204.
23. Horky, L.L., Galimi, F., Gage, F.H., and Horner, P.J. (2006). Fate of endogenous stem/progenitor cells following spinal cord injury. J. Comp. Neurol. 498, 525-538.
24. Hua, X.Y., Chen, P., Marsala, M., and Yaksh, T.L. (1999). Intrathecal substance P-induced thermal hyperalgesia and spinal release of prostaglandin E2 and amino acids. Neuroscience 89, 525-534.
25. Jorgensen, C. (2009). Link between cancer stem cells and adult mesenchymal stromal cells: Implications for cancer therapy. Regen. Med. 4, 149-152.
26. Kakinohana, O., Cizkova, D., Tomori, Z., Hedlund, E., Marsala, S., Isacson, O., and Marsala, M. (2004). Region-specific cell grafting into cervical and lumbar spinal cord in rat: A qualitative and quantitative stereological study. Exp. Neurol. 190, 122-132.
27. Kakulas, B.A. (1999). A review of the neuropathology of human spinal cord injury with emphasis on special features. J. Spinal Cord Med. 22, 119-124.
28. Karimi-Abdolrezaee, S., Eftekharpour, E., Wang, J., Morshead, C.M., and Fehlings, M.G. (2006). Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J. Neurosci. 26, 3377-3389.
29. Karmakar, M.K., Li, X., Ho, A.M., Kwok, W.H., and Chui, P.T. (2009). Real-time ultrasound-guided paramedian epidural access: Evaluation of a novel in-plane technique. Br. J. Anaesth. 102, 845-854.
30. Keirstead, H.S., Nistor, G., Bernal, G., Totoiu, M., Cloutier, F., Sharp, K., and Steward, O. (2005). Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J. Neurosci. 25, 4694-4705.
31. Liu, W.L., Lee, Y.H., Tsai, S.Y., Hsu, C.Y., Sun, Y.Y., Yang, L.Y., Tsai, S.H., and Yang, W.C. (2008). Methylprednisolone inhibits the expression of glial fibrillary acidic protein and chondroitin sulfate proteoglycans in reactivated astrocytes. Glia 56, 1390-1400.
32. Marsala, M., Hefferan, M.P., Kakinohana, O., Nakamura, S., Marsala, J., and Tomori, Z. (2005). Measurement of peripheral muscle resistance in rats with chronic ischemia-induced paraplegia or morphine-induced rigidity using a semiautomated computer-controlled muscle resistance meter. J. Neurotrauma 22, 1348-1361.
33. Marsala, M., Kakinohana, O., Yaksh, T.L., Tomori, Z., Marsala, S., and Cizkova, D. (2004). Spinal implantation of hNT neurons and neuronal precursors: Graft survival and functional effects in rats with ischemic spastic paraplegia. Eur. J. Neurosci. 20, 2401-2414.
34. Miele, V.J., Price, K.O., Bloomfield, S., Hogg, J., and Bailes, J.E. (2006). A review of intrathecal morphine therapy related granulomas. Eur. J. Pain 10, 251-261.
35. Nandoe Tewarie, R.D., Hurtado, A., Ritfeld, G.J., Rahiem, S.T., Wendell, D.F., Barroso, M.M., Grotenhuis, J.A., and Oudega, M. (2009). Bone marrow stromal cells elicit tissue sparing after acute but not delayed transplantation into the contused adult rat thoracic spinal cord. J. Neurotrauma 26, 2313-2322.
36. Oren, A., White, L.R., and Aasly, J. (2001). Apoptosis in neurones exposed to cerebrospinal fluid from patients with multiple sclerosis or acute polyradiculoneuropathy. J. Neurol. Sci. 186, 31-36.
37. Orlic, D. (2003). Adult bone marrow stem cells regenerate myocardium in ischemic heart disease. Ann. NY Acad. Sci. 996, 152-157.
38. Paul, C., Samdani, A.F., Betz, R.R., Fischer, I., and Neuhuber, B. (2009). Grafting of human bone marrow stromal cells into spinal cord injury: A comparison of delivery methods. Spine (Phila. Pa. 1976) 34, 328-334.
39. Pearse, D.D., Sanchez, A.R., Pereira, F.C., Andrade, C.M., Puzis, R., Pressman, Y., Golden, K., Kitay, B.M., Blits, B., Wood, P.M., and Bunge, M.B. (2007). Transplantation of Schwann cells and/or olfactory ensheathing glia into the contused spinal cord: Survival, migration, axon association, and functional recovery. Glia 55, 976-1000.
40. Ruitenberg, M.J., Levison, D.B., Lee, S.V., Verhaagen, J., Harvey, A.R., and Plant, G.W. (2005). NT-3 expression from engineered olfactory ensheathing glia promotes spinal sparing and regeneration. Brain 128, 839-853.
41. Safinia, N., and Minger, S.L. (2009). Generation of hepatocytes from human embryonic stem cells. Methods Mol. Biol. 481, 169-180.
42. Schwab, M.E., and Bartholdi, D. (1996). Degeneration and regeneration of axons in the lesioned spinal cord. Physiol. Rev. 76, 319-370.
43. Schwab, M.E. (2004). Nogo and axon regeneration. Curr. Opin. Neurobiol. 14, 118-124.
44. Stappenbeck, T.S., and Miyoshi, H. (2009). The role of stromal stem cells in tissue regeneration and wound repair. Science 324, 1666-1669.
45. Su, H., Zhang, W., Guo, J., Guo, A., Yuan, Q., and Wu, W. (2009). Neural progenitor cells enhance the survival and axonal regeneration of injured motoneurons after transplantation into the avulsed ventral horn of adult rats. J. Neurotrauma 26, 67-80.
46. Sykova, E., Homola, A., Mazanec, R., Lachmann, H., Konradova, S.L., Kobylka, P., Padr, R., Neuwirth, J., Komrska, V., Vavra, V., Stulik, J., and Bojar, M. (2006). Autologous bone marrow transplantation in patients with subacute and chronic spinal cord injury. Cell Transplant. 15, 675-687.
47. Sykova, E., and Jendelova, P. (2005). Magnetic resonance tracking of implanted adult and embryonic stem cells in injured brain and spinal cord. Ann. NY Acad. Sci. 1049, 146-160.
48. Vanicky, I., Urdzikova, L., Saganova, K., Cizkova, D., and Galik, J. (2001). A simple and reproducible model of spinal cord injury induced by epidural balloon inflation in the rat. J. Neurotrauma 18, 1399-1407.
49. Webber, D.J., Bradbury, E.J., McMahon, S.B., and Minger, S.L. (2007). Transplanted neural progenitor cells survive and differentiate but achieve limited functional recovery in the lesioned adult rat spinal cord. Regen. Med. 2, 929-945.
50. Wilkins, A., Kemp, K., Ginty, M., Hares, K., Mallam, E., and Scolding, N. (2009). Human bone marrow-derived mesenchymal stem cells secrete brain-derived neurotrophic factor which promotes neuronal survival in vitro. Stem Cell Res. [Epub ahead of print].
51. Yaksh, T.L. (1999). Spinal systems and pain processing: Development of novel analgesic drugs with mechanistically defined models. Trends Pharmacol. Sci. 20, 329-337.
52. Yang, H., Lu, P., McKay, H.M., Bernot, T., Keirstead, H., Steward, O., Gage, F.H., Edgerton, V.R., and Tuszynski, M.H. (2006). Endogenous neurogenesis replaces oligodendrocytes and astrocytes after primate spinal cord injury. J. Neurosci. 26, 2157-2166.
53. Zacharek, A., Chen, J., Cui, X., Li, A., Li, Y., Roberts, C., Feng, Y., Gao, Q., and Chopp, M. (2007). Angiopoietin1/Tie2 and VEGF/Flk1 induced by MSC treatment amplifies angiogenesis and vascular stabilization after stroke. J. Cereb. Blood Flow Metab. 27, 1684-1691.