Comparison of mesenchymal stem cells derived from fat, bone marrow, Wharton's jelly, and umbilical cord blood for treating spinal cord injuries in dogs

Journal of Veterinary Medical Science

Volumn 74, Issue 12, 2012, Pages 1617-1630

  Ryu, Hak Hyun ^a   Kang, Byung Jae ^a   Park, Sung Su ^a   Kim, Yongsun ^a   Sung, Gyu Jin ^a   Woo, Heung Myong ^b   Kim, Wan Hee ^a   Kweon, Oh Kyeong ^a  

^a Seoul National University   (South Korea)

^b Kangwon National University   (South Korea)

Author keywords

Canine; Mesenchymal stem cell; Spinal cord injury; Transplantation

Indexed keywords

BIOLOGICAL MARKER; COLLAGEN; CYCLOOXYGENASE 2; INTERLEUKIN 6; LAMININ; MATRIGEL; PROTEOGLYCAN;

ADIPOSE TISSUE; ANIMAL; ANIMAL DISEASE; BONE MARROW CELL; COMPARATIVE STUDY; CYTOLOGY; DOG; DRUG COMBINATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FETUS BLOOD; FLUORESCENCE; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; METHODOLOGY; NONPARAMETRIC TEST; NOTE; PATHOLOGY; PHYSIOLOGY; SPINAL CORD INJURY; SPINAL CORD REGENERATION; WESTERN BLOTTING;

ADIPOSE TISSUE; ANIMALS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; BONE MARROW CELLS; COLLAGEN; CYCLOOXYGENASE 2; DOGS; DRUG COMBINATIONS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FETAL BLOOD; FLUORESCENCE; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-6; LAMININ; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; PROTEOGLYCANS; SPINAL CORD INJURIES; SPINAL CORD REGENERATION; STATISTICS, NONPARAMETRIC;

ANIMALIA; CANIS FAMILIARIS;

EID: 84871749413     PISSN: 09167250     EISSN: 13477439     Source Type: Journal    
DOI: 10.1292/jvms.12-0065     Document Type: Note

References (54)

1. Akiyama, Y., Honmou, O., Kato, T., Uede, T., Hashi, K. and Kocsis, J. D. 2001. Transplantation of clonal neural precursor cells derived from adult human brain establishes functional peripheral myelin in the rat spinal cord. Exp. Neurol. 167: 27-39. [Medline] [CrossRef]
2. Barnett, S. C. and Riddell, J. S. 2007. Olfactory ensheathing cell transplantation as a strategy for spinal cord repair-what can it achieve? Nat. Clin. Pract. Neurol. 3: 152-161. [Medline] [CrossRef]
3. Bartholomew, A., Sturgeon, C., Siatskas, M., Ferrer, K., McIntosh, K., Patil, S., Hardy, W., Devine, S., Ucker, D., Deans, R., Moseley, A. and Hoffman, R. 2002. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp. Hematol. 30: 42-48. [Medline] [CrossRef]
4. Beck, K. D., Nguyen, H. X., Galvan, M. D., Salazar, D. L., Woodruff, T. M. and Anderson, A. J. 2010. Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain 133: 433-447. [Medline] [CrossRef]
5. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254. [Medline] [CrossRef]
6. Carlson, N. G., Rojas, M. A., Redd, J. W., Tang, P., Wood, B., Hill, K. E. and Rose, J. W. 2010. Cyclooxygenase-2 expression in oligodendrocytes increases sensitivity to excitotoxic death. J. Neuroinflammation 7: 25. [Medline] [CrossRef]
7. 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. [Medline] [CrossRef]
8. Dasari, V. R., Spomar, D. G., Gondi, C. S., Sloffer, C. A., Saving, K. L., Gujrati, M., Rao, J. S. and Dinh, D. H. 2007. Axonal remyelination by cord blood stem cells after spinal cord injury. J. Neurotrauma 24: 391-410. [Medline] [CrossRef]
9. Di Nicola, M., Carlo-Stella, C., Magni, M., Milanesi, M., Longoni, P. D., Matteucci, P., Grisanti, S. and Gianni, A. M. 2002. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99: 3838-3843. [Medline] [CrossRef]
10. Erices, A., Conget, P. and Minguell, J. J. 2000. Mesenchymal progenitor cells in human umbilical cord blood. Br. J. Haematol. 109: 235-242. [Medline] [CrossRef]
11. Fawcett, J. W. and Asher, R. A. 1999. The glial scar and central nervous system repair. Brain Res. Bull. 49: 377-391. [Medline] [CrossRef]
12. Frisen, J., Johansson, C. B., Torok, C., Risling, M. and Lendahl, U. 1995. Rapid, widespread, and longlasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J. Cell Biol. 131: 453-464. [Medline] [CrossRef]
13. Gorio, A., Torrente, Y., Madaschi, L., Di Stefano, A. B., Pisati, F., Marchesi, C., Belicchi, M., Di Giulio, A. M. and Bresolin, N. 2004. Fate of autologous dermal stem cells transplanted into the spinal cord after traumatic injury (TSCI). Neuroscience 125: 179-189. [Medline] [CrossRef]
14. Han, H. J., Sigurdson, W. J., Nickerson, P. A. and Taub, M. 2004. Both mitogen activated protein kinase and the mammalian target of rapamycin modulate the development of functional renal proximal tubules in matrigel. J. Cell Sci. 117: 1821-1833. [Medline] [CrossRef]
15. Hardy, S. A., Maltman, D. J. and Przyborski, S. A. 2008. Mesenchymal stem cells as mediators of neural differentiation. Curr. Stem Cell Res. Ther. 3: 43-52. [Medline] [CrossRef]
16. Hauner, H., Entenmann, G., Wabitsch, M., Gaillard, D., Ailhaud, G., Negrel, R. and Pfeiffer, E. F. 1989. Promoting effect of glucocorticoids on the differentiation of human adipocyte precursor cells cultured in a chemically defined medium. J. Clin. Invest. 84: 1663-1670. [Medline] [CrossRef]
17. 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. U.S.A. 99: 2199-2204. [Medline] [CrossRef]
18. Johansson, C. B., Momma, S., Clarke, D. L., Risling, M., Lendahl, U. and Frisen, J. 1999. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96: 25-34. [Medline] [CrossRef]
19. Kang, S. K., Shin, M. J., Jung, J. S., Kim, Y. G. and Kim, C. H. 2006. Autologous adipose tissue-derived stromal cells for treatment of spinal cord injury. Stem Cells Dev. 15: 583-594. [Medline] [CrossRef]
20. Kleinman, H. K., McGarvey, M. L., Hassell, J. R., Star, V. L., Cannon, F. B., Laurie, G. W. and Martin, G. R. 1986. Basement membrane complexes with biological activity. Biochemistry 25: 312-318. [Medline] [CrossRef]
21. Koh, S. H., Kim, K. S., Choi, M. R., Jung, K. H., Park, K. S., Chai, Y. G., Roh, W., Hwang, S. J., Ko, H. J., Huh, Y. M., Kim, H. T. and Kim, S. H. 2008. Implantation of human umbilical cordderived mesenchymal stem cells as a neuroprotective therapy for ischemic stroke in rats. Brain Res. 1229: 233-248. [Medline] [CrossRef]
22. Llado, J., Haenggeli, C., Maragakis, N. J., Snyder, E. Y. and Rothstein, J. D. 2004. Neural stem cells protect against glutamate-induced excitotoxicity and promote survival of injured motor neurons through the secretion of neurotrophic factors. Mol. Cell. Neurosci. 27: 322-331. [Medline] [CrossRef]
23. Lu, P., Blesch, A. and Tuszynski, M. H. 2004. Induction of bone marrow stromal cells to neurons: differentiation, transdifferentiation, or artifact? J. Neurosci. Res. 77: 174-191. [Medline] [CrossRef]
24. McTigue, D. M., Tani, M., Krivacic, K., Chernosky, A., Kelner, G. S., Maciejewski, D., Maki, R., Ransohoff, R. M. and Stokes, B. T. 1998. Selective chemokine mRNA accumulation in the rat spinal cord after contusion injury. J. Neurosci. Res. 53: 368-376. [Medline]
25. Mirza, B., Krook, H., Andersson, P., Larsson, L. C., Korsgren, O. and Widner, H. 2004. Intracerebral cytokine profiles in adult rats grafted with neural tissue of different immunological disparity. Brain Res. Bull. 63: 105-118. [Medline] [CrossRef]
26. Okada, S., Nakamura, M., Mikami, Y., Shimazaki, T., Mihara, M., Ohsugi, Y., Iwamoto, Y., Yoshizaki, K., Kishimoto, T., Toyama, Y. and Okano, H. 2004. Blockade of interleukin-6 receptor suppresses reactive astrogliosis and ameliorates functional recovery in experimental spinal cord injury. J. Neurosci. Res. 76: 265-276. [Medline] [CrossRef]
27. Okano, H. 2002. Stem cell biology of the central nervous system. J. Neurosci. Res. 69: 698-707. [Medline] [CrossRef]
28. Park, S. S., Byeon, Y. E., Ryu, H. H., Kang, B. J., Kim, Y., Kim, W. H., Kang, K. S., Han, H. J. and Kweon, O. K. 2011. Comparison of canine umbilical cord blood-derived mesenchymal stem cell transplantation times: involvement of astrogliosis, inflammation, intracellular actin cytoskeleton pathways, and neurotrophin. Cell Transplant. 20: 1867-1880. [Medline]
29. Parr, A. M., Kulbatski, I. and Tator, C. H. 2007. Transplantation of adult rat spinal cord stem/progenitor cells for spinal cord injury. J. Neurotrauma 24: 835-845. [Medline] [CrossRef]
30. Parr, A. M., Kulbatski, I., Wang, X. H., Keating, A. and Tator, C. H. 2008. Fate of transplanted adult neural stem/progenitor cells and bone marrow-derived mesenchymal stromal cells in the injured adult rat spinal cord and impact on functional recovery. Surg. Neurol. 70: 600-607. [Medline] [CrossRef]
31. Pearse, D. D. and Bunge, M. B. 2006. Designing celland genebased regeneration strategies to repair the injured spinal cord. J. Neurotrauma 23: 438-452. [Medline] [CrossRef]
32. Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S. and Marshak, D. R. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147. [Medline] [CrossRef]
33. Popovich, P. G., Wei, P. and Stokes, B. T. 1997. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J. Comp. Neurol. 377: 443-464. [Medline] [CrossRef]
34. Rabinowitz, R. S., Eck, J. C., Harper, C. M. Jr., Larson, D. R., Jimenez, M. A., Parisi, J. E., Friedman, J. A., Yaszemski, M. J. and Currier, B. L. 2008. Urgent surgical decompression compared to methylprednisolone for the treatment of acute spinal cord injury: a randomized prospective study in beagle dogs. Spine (Phila Pa 1976) 33: 2260-2268. [Medline] [CrossRef]
35. Reyes, M., Lund, T., Lenvik, T., Aguiar, D., Koodie, L. and Verfaillie, C. M. 2001. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 98: 2615-2625. [Medline] [CrossRef]
36. Ryu, H. H., Lim, J. H., Byeon, Y. E., Park, J. R., Seo, M. S., Lee, Y. W., Kim, W. H., Kang, K. S. and Kweon, O. K. 2009. Functional recovery and neural differentiation after transplantation of allogenic adipose-derived stem cells in a canine model of acute spinal cord injury. J. Vet. Sci. 10: 273-284. [Medline] [CrossRef]
37. Safford, K. M., Hicok, K. C., Safford, S. D., Halvorsen, Y. D., Wilkison, W. O., Gimble, J. M. and Rice, H. E. 2002. Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem. Biophys. Res. Commun. 294: 371-379. [Medline] [CrossRef]
38. Sasaki, M., Radtke, C., Tan, A. M., Zhao, P., Hamada, H., Houkin, K., Honmou, O. and Kocsis, J. D. 2009. BDNF-hypersecreting human mesenchymal stem cells promote functional recovery, axonal sprouting, and protection of corticospinal neurons after spinal cord injury. J. Neurosci. 29: 14932-14941. [Medline] [CrossRef]
39. Scheff, S. W., Rabchevsky, A. G., Fugaccia, I., Main, J. A. and Lumpp, J. E. Jr. 2003. Experimental modeling of spinal cord injury: characterization of a force-defined injury device. J. Neurotrauma 20: 179-193. [Medline] [CrossRef]
40. Seo, M. S., Jeong, Y. H., Park, J. R., Park, S. B., Rho, K. H., Kim, H. S., Yu, K. R., Lee, S. H., Jung, J. W., Lee, Y. S. and Kang, K. S. 2009. Isolation and characterization of canine umbilical cord blood-derived mesenchymal stem cells. J. Vet. Sci. 10: 181-187. [Medline] [CrossRef]
41. Shetty, P., Cooper, K. and Viswanathan, C. 2010. Comparison of proliferative and multilineage differentiation potentials of cord matrix, cord blood, and bone marrow mesenchymal stem cells. Asian J. Transfus. Sci. 4: 14-24. [Medline] [CrossRef]
42. Shuman, S. L., Bresnahan, J. C. and Beattie, M. S. 1997. Apoptosis of microglia and oligodendrocytes after spinal cord contusion in rats. J. Neurosci. Res. 50: 798-808. [Medline] [CrossRef]
43. Siegenthaler, M. M., Tu, M. K. and Keirstead, H. S. 2007. The extent of myelin pathology differs following contusion and transection spinal cord injury. J. Neurotrauma 24: 1631-1646. [Medline] [CrossRef]
44. Silver, J. and Miller, J. H. 2004. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5: 146-156. [Medline] [CrossRef]
45. Swanger, S. A., Neuhuber, B., Himes, B. T., Bakshi, A. and Fischer, I. 2005. Analysis of allogeneic and syngeneic bone marrow stromal cell graft survival in the spinal cord. Cell Transplant. 14: 775-786. [Medline] [CrossRef]
46. Sykova, E. and Jendelova, P. 2005. Magnetic resonance tracking of implanted adult and embryonic stem cells in injured brain and spinal cord. Ann. N. Y. Acad. Sci. 1049: 146-160. [Medline] [CrossRef]
47. Taub, M., Wang, Y., Szczesny, T. M. and Kleinman, H. K. 1990. Epidermal growth factor or transforming growth factor alpha is required for kidney tubulogenesis in matrigel cultures in serumfree medium. Proc. Natl. Acad. Sci. U.S.A. 87: 4002-4006. [Medline] [CrossRef]
48. Troyer, D. L. and Weiss, M. L. 2008. Wharton's jelly-derived cells are a primitive stromal cell population. Stem Cells 26: 591-599. [Medline] [CrossRef]
49. Uemura, M., Refaat, M. M., Shinoyama, M., Hayashi, H., Hashimoto, N. and Takahashi, J. 2010. Matrigel supports survival and neuronal differentiation of grafted embryonic stem cell-derived neural precursor cells. J. Neurosci. Res. 88: 542-551. [Medline]
50. Wagner, W., Wein, F., Seckinger, A., Frankhauser, M., Wirkner, U., Krause, U., Blake, J., Schwager, C., Eckstein, V., Ansorge, W. and Ho, A. D. 2005. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp. Hematol. 33: 1402-1416. [Medline]
51. Webb, A. A., Jeffery, N. D., Olby, N. J. and Muir, G. D. 2004. Behavioural analysis of the efficacy of treatments for injuries to the spinal cord in animals. Vet. Rec. 155: 225-230. [CrossRef]
52. Yang, C. C., Shih, Y. H., Ko, M. H., Hsu, S. Y., Cheng, H. and Fu, Y. S. 2008. Transplantation of human umbilical mesenchymal stem cells from Wharton's jelly after complete transection of the rat spinal cord. PLoS ONE 3: e3336. [Medline] [CrossRef]
53. Zai, L. J. and Wrathall, J. R. 2005. Cell proliferation and replacement following contusive spinal cord injury. Glia 50: 247-257. [Medline] [CrossRef]
54. Zhang, H. T., Cheng, H. Y., Cai, Y. Q., Ma, X., Liu, W. P., Yan, Z. J., Jiang, X. D. and Xu, R. X. 2009. Comparison of adult neurospheres derived from different origins for treatment of rat spinal cord injury. Neurosci. Lett. 458: 116-121. [Medline] [CrossRef]