Human mesenchymal stem cells modulate inflammatory cytokines after spinal cord injury in rat

International Journal of Molecular Sciences

Volumn 15, Issue 7, 2014, Pages 11275-11293

  Urdzíková, Lucia Machová ^a   Růžička, Jiří ^a,b   LaBagnara, Michael ^c   Kárová, Kristýna ^a,b   Kubinová, Šárka ^a   Jiráková, Klára ^a   Murali, Raj ^c   Syková, Eva ^a,b   Jhanwar Uniyal, Meena ^c   Jendelová, Pavla ^a,b  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Inflammatory cytokines; Mesenchymal stem cells; Spinal cord injury

Indexed keywords

AZATHIOPRINE; CYCLOSPORIN A; FIBROBLAST GROWTH FACTOR 2; GENTAMICIN; INTERFERON REGULATORY FACTOR 5; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; TUMOR NECROSIS FACTOR ALPHA; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOGLOBULIN RECEPTOR; INTERFERON REGULATORY FACTOR; INTERLEUKIN DERIVATIVE; NEUROMODULIN; RANTES;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASSO BEATTIE AND BRESNAHAN TEST; CELL SURVIVAL; CELL TRANSPLANTATION; CONTROLLED STUDY; EXPERIMENTAL BEHAVIORAL TEST; FLAT BEAM TEST; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MESENCHYMAL STEM CELL; MORPHOMETRICS; NERVE SPROUTING; NONHUMAN; PLANTAR TEST; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPINAL CORD INJURY; WHITE MATTER; ANIMAL; GENETICS; HUMAN; LOCOMOTION; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; SPINAL CORD INJURIES; WISTAR RAT;

ANIMALS; CHEMOKINE CCL5; FIBROBLAST GROWTH FACTOR 2; GAP-43 PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; INTERFERON REGULATORY FACTORS; INTERLEUKINS; LOCOMOTION; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; RATS; RATS, WISTAR; RECEPTORS, IMMUNOLOGIC; SPINAL CORD INJURIES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84903397419     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms150711275     Document Type: Article

References (39)

1. Oliveri, R. S.; Bello, S.; Biering-Sorensen, F. Mesenchymal stem cells improve locomotor recovery in traumatic spinal cord injury: Systematic review with meta-analyses of rat models. Neurobiol. Dis. 2014, 62, 338-353.
2. Urdzikova, L.; Jendelova, P.; Glogarova, K.; Burian, M.; Hajek, M.; Sykova, E. Transplantation of bone marrow stem cells as well as mobilization by granulocyte-colony stimulating factor promotes recovery after spinal cord injury in rats. J. Neurotrauma 2006, 23, 1379-1391.
3. Coutts, M.; Keirstead, H. S. Stem cells for the treatment of spinal cord injury. Exp. Neurol. 2008, 209, 368-377.
4. Garbuzova-Davis, S.; Willing, A. E.; Saporta, S.; Bickford, P. C.; Gemma, C.; Chen, N.; Sanberg, C. D.; Klasko, S. K.; Borlongan, C. V.; Sanberg, P. R. Novel cell therapy approaches for brain repair. Prog. Brain Res. 2006, 157, 207-222.
5. Joyce, N.; Annett, G.; Wirthlin, L.; Olson, S.; Bauer, G.; Nolta, J. A. Mesenchymal stem cells for the treatment of neurodegenerative disease. Regen. Med. 2010, 5, 933-946.
6. Hardy, S. A.; Maltman, D. J.; Przyborski, S. A. Mesenchymal stem cells as mediators of neural differentiation. Curr. Stem Cell Res. Ther. 2008, 3, 43-52.
7. Nishio, Y.; Koda, M.; Kamada, T.; Someya, Y.; Yoshinaga, K.; Okada, S.; Harada, H.; Okawa, A.; Moriya, H.; Yamazaki, M. The use of hemopoietic stem cells derived from human umbilical cord blood to promote restoration of spinal cord tissue and recovery of hindlimb function in adult rats. J. Neurosurg. Spine 2006, 5, 424-433.
8. English, K. Mechanisms of mesenchymal stromal cell immunomodulation. Immunol. Cell Biol. 2013, 91, 19-26.
9. Stagg, J.; Galipeau, J. Mechanisms of immune modulation by mesenchymal stromal cells and clinical translation. Curr. Mol. Med. 2013, 13, 856-867.
10. Weiss, D. J.; Casaburi, R.; Flannery, R.; LeRoux-Williams, M.; Tashkin, D. P. A placebo-controlled, randomized trial of mesenchymal stem cells in copd. Chest 2013, 143, 1590-1598.
11. Karussis, D.; Karageorgiou, C.; Vaknin-Dembinsky, A.; Gowda-Kurkalli, B.; Gomori, J. M.; Kassis, I.; Bulte, J. W.; Petrou, P.; Ben-Hur, T.; Abramsky, O.; et al. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch. Neurol. 2010, 67, 1187-1194.
12. Vanecek, V.; Zablotskii, V.; Forostyak, S.; Ruzicka, J.; Herynek, V.; Babic, M.; Jendelova, P.; Kubinova, S.; Dejneka, A.; Sykova, E. Highly efficient magnetic targeting of mesenchymal stem cells in spinal cord injury. Int. J. Nanomed. 2012, 7, 3719-3730.
13. Zhilai, Z.; Hui, Z.; Anmin, J.; Shaoxiong, M.; Bo, Y.; Yinhai, C. A combination of taxol infusion and human umbilical cord mesenchymal stem cells transplantation for the treatment of rat spinal cord injury. Brain Res. 2012, 1481, 79-89.
14. Cizkova, D.; Novotna, I.; Slovinska, L.; Vanicky, I.; Jergova, S.; Rosocha, J.; Radonak, J. Repetitive intrathecal catheter delivery of bone marrow mesenchymal stromal cells improves functional recovery in a rat model of contusive spinal cord injury. J. Neurotrauma 2011, 28, 1951-1961.
15. Mothe, A. J.; Bozkurt, G.; Catapano, J.; Zabojova, J.; Wang, X.; Keating, A.; Tator, C. H. Intrathecal transplantation of stem cells by lumbar puncture for thoracic spinal cord injury in the rat. Spinal Cord 2011, 49, 967-973.
16. Basso, D. M.; Beattie, M. S.; Bresnahan, J. C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 1995, 12, 1-21.
17. Hodgetts, S. I.; Simmons, P. J.; Plant, G. W. Human mesenchymal precursor cells (stro-1(+) from spinal cord injury patients improve functional recovery and tissue sparing in an acute spinal cord injury rat model. Cell Transplant. 2013, 22, 393-412.
18. Ritfeld, G. J.; Nandoe Tewarie, R. D.; Vajn, K.; Rahiem, S. T.; Hurtado, A.; Wendell, D. F.; Roos, R. A.; Oudega, M. Bone marrow stromal cell-mediated tissue sparing enhances functional repair after spinal cord contusion in adult rats. Cell Transplant. 2012, 21, 1561-1575.
19. Urdzikova, L.; Vanicky, I. Post-traumatic moderate systemic hyperthermia worsens behavioural outcome after spinal cord injury in the rat. Spinal Cord 2006, 44, 113-119.
20. Amemori, T.; Jendelova, P.; Ruzickova, K.; Arboleda, D.; Sykova, E. Co-transplantation of olfactory ensheathing glia and mesenchymal stromal cells does not have synergistic effects after spinal cord injury in the rat. Cytotherapy 2010, 12, 212-225.
21. Arboleda, D.; Forostyak, S.; Jendelova, P.; Marekova, D.; Amemori, T.; Pivonkova, H.; Masinova, K.; Sykova, E. Transplantation of predifferentiated adipose-derived stromal cells for the treatment of spinal cord injury. Cell. Mol. Neurobiol. 2011, 31, 1113-1122.
22. Pourheydar, B.; Joghataei, M. T.; Bakhtiari, M.; Mehdizadeh, M.; Yekta, Z.; Najafzadeh, N. Co-transplantation of bone marrow stromal cells with schwann cells evokes mechanical allodynia in the contusion model of spinal cord injury in rats. Cell J. 2012, 13, 213-222.
23. Paul, C.; Samdani, A. F.; Betz, R. R.; Fischer, I.; Neuhuber, B. Grafting of human bone marrow stromal cells into spinal cord injury: A comparison of delivery methods. Spine 2009, 34, 328-334.
24. Hejcl, A.; Ruzicka, J.; Kapcalova, M.; Turnovcova, K.; Krumbholcova, E.; Pradny, M.; Michalek, J.; Cihlar, J.; Jendelova, P.; Sykova, E. Adjusting the chemical and physical properties of hydrogels leads to improved stem cell survival and tissue ingrowth in spinal cord injury reconstruction: A comparative study of four methacrylate hydrogels. Stem Cells Dev. 2013, 22, 2794-2805.
25. Hejcl, A.; Sedy, J.; Kapcalova, M.; Toro, D. A.; Amemori, T.; Lesny, P.; Likavcanova-Masinova, K.; Krumbholcova, E.; Pradny, M.; Michalek, J.; et al. Hpma-rgd hydrogels seeded with mesenchymal stem cells improve functional outcome in chronic spinal cord injury. Stem Cells Dev. 2010, 19, 1535-1546.
26. Renault-Mihara, F.; Okada, S.; Shibata, S.; Nakamura, M.; Toyama, Y.; Okano, H. Spinal cord injury: Emerging beneficial role of reactive astrocytes' migration. Int. J. Biochem. Cell Biol. 2008, 40, 1649-1653.
27. Lukovic, D.; Moreno Manzano, V.; Stojkovic, M.; Bhattacharya, S. S.; Erceg, S. Concise review: Human pluripotent stem cells in the treatment of spinal cord injury. Stem Cells 2012, 30, 1787-1792.
28. Hausmann, O. N. Post-traumatic inflammation following spinal cord injury. Spinal Cord 2003, 41, 369-378.
29. Cusimano, M.; Biziato, D.; Brambilla, E.; Donega, M.; Alfaro-Cervello, C.; Snider, S.; Salani, G.; Pucci, F.; Comi, G.; Garcia-Verdugo, J. M.; et al. Transplanted neural stem/precursor cells instruct phagocytes and reduce secondary tissue damage in the injured spinal cord. Brain 2012, 135, 447-460.
30. Ren, Y.; Young, W. Managing inflammation after spinal cord injury through manipulation of macrophage function. Neural Plast. 2013, 2013, 945034.
31. Hirai, T.; Uchida, K.; Nakajima, H.; Guerrero, A. R.; Takeura, N.; Watanabe, S.; Sugita, D.; Yoshida, A.; Johnson, W. E.; Baba, H. The prevalence and phenotype of activated microglia/macrophages within the spinal cord of the hyperostotic mouse (twy/twy) changes in response to chronic progressive spinal cord compression: Implications for human cervical compressive myelopathy. PLoS One 2013, 8, e64528.
32. Krausgruber, T.; Blazek, K.; Smallie, T.; Alzabin, S.; Lockstone, H.; Sahgal, N.; Hussell, T.; Feldmann, M.; Udalova, I. A. Irf5 promotes inflammatory macrophage polarization and th1-th17 responses. Nat. Immunol. 2011, 12, 231-238.
33. Nakajima, H.; Uchida, K.; Rodriguez Guerrero, A.; Watanabe, S.; Sugita, D.; Takeura, N.; Yoshida, A.; Long, G.; Wright, K.; Johnson, E.; et al. Transplantation of mesenchymal stem cells promotes the alternative pathway of macrophage activation and functional recovery after spinal cord injury. J. Neurotrauma 2012, 29, 1614-1625.
34. Greish, S.; Abogresha, N.; Abdel-Hady, Z.; Zakaria, E.; Ghaly, M.; Hefny, M. Human umbilical cord mesenchymal stem cells as treatment of adjuvant rheumatoid arthritis in a rat model. World J. Stem Cells 2012, 4, 101-109.
35. Kim, J.; Hematti, P. Mesenchymal stem cell-educated macrophages: A novel type of alternatively activated macrophages. Exp. Hematol. 2009, 37, 1445-1453.
36. Li, M.; Ikehara, S. Bone-marrow-derived mesenchymal stem cells for organ repair. Stem Cells Int. 2013, 2013, 1-8.
37. De la Calle, J. L.; Paino, C. L. A procedure for direct lumbar puncture in rats. Brain Res. Bull. 2002, 59, 245-250.
38. Machova Urdzikova, L.; Sedlacek, R.; Suchy, T.; Amemori, T.; Ruzicka, J.; Lesny, P.; Havlas, V.; Sykova, E.; Jendelova, P. Human multipotent mesenchymal stem cells improve healing after collagenase tendon injury in the rat. Biomed. Eng. Online 2014, 13, 42.
39. Goldstein, B.; Little, J. W.; Harris, R. M. Axonal sprouting following incomplete spinal cord injury: An experimental model. J. Spinal Cord Med. 1997, 20, 200-206.