Long-lasting effects of human mesenchymal stem cell systemic administration on pain-like behaviors, cellular, and biomolecular modifications in neuropathic mice

Frontiers in Integrative Neuroscience

Volumn , Issue DECEMBER, 2011, Pages

  Siniscalco, Dario ^a   Giordano, Catia ^a   Galderisi, Umberto ^a   Luongo, Livio ^a   de Novellis, Vito ^a   Rossi, Francesco ^a   Maione, Sabatino ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Cell transplantation; Human mesenchymal stem cells; Macrophages; Neuropathic pain

Indexed keywords

5' NUCLEOTIDASE; BETA TUBULIN; CD4 ANTIGEN; CELL MARKER; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOSYLPHOSPHATIDYLINOSITOL; IBA 1 PROTEIN; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTINOCICEPTION; ARTICLE; ASTROCYTE; BEHAVIOR; CD4+ T LYMPHOCYTE; CELL CONTACT; CELL HOMING; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE MODEL; GENE; GENE EXPRESSION; GLYCERALDEHYDE PHOSPHATE DEHYDROGENASE GENE; HUMAN; HUMAN CELL; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; INJECTION; INTRAVENOUS ADMINISTRATION; MACROPHAGE ACTIVATION; MALE; MECHANICAL ALLODYNIA; MESENCHYMAL STEM CELL TRANSPLANTATION; MOTOR COORDINATION; MOTOR PERFORMANCE; MOUSE; NERVE INJURY; NEUROPATHIC PAIN; NONHUMAN; PREFRONTAL CORTEX; PROTEIN EXPRESSION; SCIATIC NERVE; SPARED NERVE INJURY; SPINAL CORD; THERMAL HYPERALGESIA; TREATMENT OUTCOME;

EID: 84855285104     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2011.00079     Document Type: Article

References (62)

1. Ankrum, J., and Karp, J. M. (2010). Mesenchymal stem cell therapy: two steps forward, one step back. Trends. Mol. Med. 16, 203-209.
2. Beggs, K. J., Lyubimov, A., Borneman, J. N., Bartholomew, A., Moseley, A., Dodds, R., Archambault, M. P., Smith, A. K., and McIntosh, K. R. (2006). Immunologic consequences of multiple, high-dose administra-tionof allogeneicmesenchymalstem cells to baboons. Cell Transplant. 15, 711-721.
3. Beyth, S., Borovsky, Z., Mevorach, D., Liebergall, M., Gazit, Z., Aslan, H., Galun, E., and Rachmilewitz, J. (2005). Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 105, 2214-2219.
4. Bonfield, T. L., and Caplan, A. I. (2010). Adult mesenchymal stem cells: an innovative therapeutic for lung diseases. Discov. Med. 9, 337-345.
5. Bourquin, A. F., Süveges, M., Pertin, M., Gilliard, N., Sardy, S., Davison, A. C., Spahn, D. R., and Decosterd, I. (2006). Assessment and analysis of mechanical allodynia-like behav-ior induced by spared nerve injury (SNI) in the mouse. Pain 122, 14.e1-14.e14.
6. Bradford, M. M. (1976). A rapid and sensitive method for the quanti-zation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72,248-254.
7. Cao, Q., Benton, R. L., and Whitte-more, S. R. (2002). Stem cell repair of central nervous system injury. J. Neurosci. Res. 68, 501-510.
8. Caplan, A. I. (2009). Why are MSCs therapeutic? New data: new insight. J. Pathol. 217, 318-324.
9. Ceradini, D. J., Kulkarni, A. R., Callaghan, M. J., Tepper, O. M., Bastidas, N., Kleinman, M. E., Capla, J. M., Galiano, R. D., Levine, J. P., and Gurtner, G. C. (2004). Prog-enitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SCF-1. Nat. Med. 10, 858-864.
10. Corcione, A., Benvenuto, F., Ferretti, E., Giunti, D., Cappiello, V., Cazzanti, F., Risso, M., Gualandi, F., Man-cardi, G. L., Pistoia, V., and Uccelli, A. (2006). Human mesenchymal stemcellsmodulateB-cellfunctions. Blood 107, 367-372.
11. Dazzi, F., and Marelli-Berg, F. M.(2008). Mesenchymal stem cells for graft-versus-hostdisease:closeencounters with T cells. Eur. J. Immunol. 38, 1479-1482.
12. de Novellis, V., Siniscalco, D., Galderisi, U., Fuccio, C., Nolano, M., San-toro, L., Cascino, A., Roth, K. A., Rossi, F., and Maione, S. (2004). Blockadeof glutamatemGlu5recep-tors in a rat model of neuropathic pain prevents early over-expression of pro-apoptotic genes and mor-phological changes in dorsal horn lamina II. Neuropharmacology 46, 468-479.
13. 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-lymphocyteproliferationinducedby cellular or nonspecific mitogenic stimuli. Blood 99, 3838-3843.
14. Forte, A., Finicelli, M., Mattia, M., Berrino, L., Rossi, F., De Feo, M., Cotrufo, M., Cipollaro, M., Cas-cino, A., and Galderisi, U. (2008). Mesenchymal stem cells effectively reduce surgically induced stenosis in rat carotids. J. Cell. Physiol. 217, 789-799.
15. Fuccio, C., Luongo, C., Capodanno, P., Giordano, C., Scafuro, M. A., Siniscalco, D., Lettieri, B., Rossi, F., Maione, S., and Berrino, L. (2009). A single subcutaneous injec-tion of ozone prevents allodynia and decreases the over-expression of pro-inflammatory caspases in the orbito-frontal cortex of neuropathic mice. Eur. J. Pharmacol. 603, 42-49.
16. Galluzi, K. E. (2005). Management of neuropathic pain. J. Am. Osteopath. Assoc. 105, 12-19.
17. Gao, J., Dennis, J. E., Muzic, R. F., Lund-berg, M., and Caplan, A. I. (2001). The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. CellsTissues Organs (Print) 169, 12-20.
18. Giordano, A., Galderisi, U., and Marino, I. R. (2007). From the laboratory bench to the patient's bedside: an update on clinical trials with mes-enchymal stem cells. J. Cell. Physiol. 211,27-35.
19. Gur-Wahnon, D., Borovsky, Z., Beyth, S., Liebergall, M., and Rachmile-witz, J. (2007). Contact-dependent induction of regulatory antigen-presenting cells by human mes-enchymal stem cells is mediated via STAT3 signaling. Exp. Hematol. 35, 426-433.
20. Gur-Wahnon, D., Borovsky, Z., Lieber-gall, M., and Rachmilewitz, J.(2009). Theinductionof APCwithadistinct tolerogenic phenotype via contact-dependent STAT3 activation. PLoS ONE 4, e6846. doi:10.1371/jour-nal.pone.0006846
21. Hoogduijn, M. J., Popp, F., Verbeek, R., Masoodi, M., Nicolaou, A., Baan, C., and Dahlke, M. H. (2010). The immunomodulatory properties of mesenchymal stem cells and their use for immunotherapy. Int. Immunopharmacol. 10, 1496-1500.
22. Jasmin, L., Rabkin, S. D., Granato, A., Boudah, A., and Ohara, P. T. (2003). Analgesia and hyperalgesia from GABA-mediated modulation of the cerebral cortex. Nature 424, 316-320.
23. Kiguchi, N., Maeda, T., Kobayashi, Y., Fukazawa, Y., and Kishioka, S. (2010). Macrophage inflam-matory protein-1alpha mediates the development of neuropathic pain following peripheral nerve injury through interleukin-1beta up-regulation. Pain 149, 305-315.
24. Kim, J., and Hematti, P. (2009). Mesenchymal stem cell-educated macrophages: a novel type of alter-nativelyactivatedmacrophages. Exp. Hematol. 37, 1445-1453.
25. Klass, M., Gavrikov, V., Drury, D., Stewart, B., Hunter, S., Denson, D. D., Hord, A., and Csete, M. (2007). Intravenous mononu-clear marrow cells reverse neu-ropathic pain from experimen-tal mononeuropathy. Anesth. Analg. 104,944-948.
26. Kleinschnitz, C., Hofstetter, H. H., Meuth, S. G., Braeuninger, S., Som-mer, C., and Stoll, G. (2006). T cell infiltration after chronic con-striction injury of mouse sciatic nerve is associated with interleukin-17 expression. Exp. Neurol. 200, 480-485.
27. Le Blanc, K., and Pittenger, M. (2005). Mesenchymal stem cells: progress toward promise. Cytotherapy 7, 36-45.
28. Lee, R. H., Pulin, A. A., Seo, M. J., Kota, D. J., Ylostalo, J., Larson, B. L., Semprun-Prieto, L., Delafontaine, P., and Prockop, D. J. (2009). Intra-venous hMSCs improve myocar-dial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 5, 54-63.
29. Lindvall, O., and Kokaia, Z. (2005). Stem cell therapy for human brain disorders. KidneyInt.68,1937-1939.
30. Lindvall, O., and Kokaia, Z. (2006). Stem cells for the treatment of neurological disorders. Nature 441, 1094-1096.
31. Maeda, T., Kiguchi, N., Kobayashi, Y., Ikuta, T., Ozaki, M., and Kish-ioka, S. (2009). Leptin derived from adipocytes in injured peripheral nerves facilitates development of neuropathic pain via macrophage stimulation. Proc. Natl. Acad. Sci. U.S.A. 106, 13076-13081.
32. Mahmood, A., Lu, D., and Chopp, M. (2004). Intravenous administration of marrow stromal cells (MSCs) increases the expression of growth factors in rat brain after traumatic brain injury. J. Neurotrauma 21, 33-39.
33. Maione, S., Siniscalco, D., Galderisi, U., de Novellis, V., Uliano, R., Di Bernardo, G., Berrino, L., Cascino, A., and Rossi, F. (2002). Apoptotic genes expression in the lumbar dor-salhorninamodelneuropathicpain in rat. Neuroreport 13, 101-106.
34. Mattsson, J. (2008). Recent progress in allogeneic stem cell transplantation. Curr. Opin. Mol. Ther. 10, 343-349.
35. Meirelles Lda, S., Fontes, A. M., Covas, D.T., and Caplan, A.I.(2009).Mech-anisms involved in the therapeu-tic properties of mesenchymal stem cells. Cytokine Growth Factor Rev. 20, 419-427.
36. Merskey, H., and Bogduk, N. (1994). Classification of Chronic Pain. Seat-tle: IASP Press.
37. Mika, J., Rojewska, E., Makuch, W., and Przewlocka, B. (2010). Minocycline reduces the injury-induced expres-sion of prodynorphin and pronoci-ceptin in the dorsal root ganglion in a rat model of neuropathic pain. Neuroscience 165, 1420-1428.
38. Musolino, P. L., Coronel, M. F., Hok-felt, T., and Villar, M. J. (2007). Bone marrow stromal cells induce changes in pain behavior after sciatic nerve constriction. Neurosci. Lett. 418,97-101.
39. Nauta, A. J., and Fibbe, W. E. (2007). Immunomodulatory properties of mesenchymal stromal cells. Blood 110,3499-3506.
40. Neugebauer, V., Galhardo, V., Maione, S., and Mackey, S. C. (2009). Fore-brain pain mechanisms. Brain Res. Rev. 60, 226-242.
41. Otoshi, K., Kikuchi, S., Konno, S., and Sekiguchi, M. (2010). The reac-tions of glial cells and endoneur-ial macrophages in the dorsal root ganglion and their contribution to pain-related behavior after applica-tion of nucleus pulposus onto the nerve root in rats. Spine 35, 10-17.
42. Pan, H. C., Cheng, F. C., Chen, C. J., Lai, S. Z., Lee, C. W., Yang, D. Y., Chang, M. H., and Ho, S. P. (2007). Post-injury regeneration in rat sciatic nerve facilitated by neu-rotrophic factors secreted by amni-otic fluid mesenchymal stem cells. J. Clin. Neurosci. 14, 1089-1098.
43. Petrie Aronin, C. E., and Tuan, R. S. (2010). Therapeutic potential of the immunomodulatory activities of adult mesenchymal stem cells. Birth Defects Res. C Embryo Today 90, 67-74.
44. Pisati, F., Bossolasco, P., Meregalli, M., Cova, L., Belicchi, M., Gav-ina, M., Marchesi, C., Calzarossa, C., Soligo, D., Lambertenghi-Deliliers, G., Bresolin, N., Silani, V., Tor-rente, Y., and Polli, E. (2007). Induc-tion of neurotrophin expression via human adult mesenchymal stem cells: implication for cell therapy in neurodegenerative diseases. Cell Transplant. 16, 41-55.
45. Porcheray, F., Viaud, S., Rimaniol, A. C., Léone, C., Samah, B., Dereuddre-Bosquet, N., Dormont, D., and Gras, G. (2005). Macrophage activation switching: an asset for the reso-lution of inflammation. Clin. Exp. Immunol. 142, 481-489.
46. Pricola, K. L., Kuhn, N. Z., Haleem-Smith, H., Song, Y., and Tuan, R. S. (2009). Interleukin-6 main-tains bone marrow-derived mes-enchymal stem cell stemness by an ERK1/2-dependent mechanism. J. Cell. Biochem. 108, 577-588.
47. Sarugaser, R., Lickorish, D., Baksh, D., Hosseini, M. M., and Davies, J. E. (2005). Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells 23, 220-229.
48. Schipani, E., and Kronenberg, H. M. (2009). Adult mesenchymal stem cells, in StemBook, Edn. The Stem Cell Research Commu-nity, Eds K. R. Chien, (Cambridge, MA: Harvard Stem Cell Institute), doi/10.3824/stembook.1.38.1
49. Scholz, J., and Woolf, C. J. (2007). Theneuropathicpaintriad:neurons, immunecellsandglia. Nat.Neurosci. 10,1361-1368.
50. Siniscalco, D. (2010). Transplantation of human mesenchymal stem cells in the study of neuropathic pain. Methods Mol. Biol. 617, 337-345.
51. Siniscalco, D., de Novellis, V., Rossi, F., and Maione, S. (2005a). Neuro-pathic pain: is the end of suffering starting in the gene therapy? Curr. Drug Targets 6, 75-80.
52. Siniscalco, D., Fuccio, C., de Novellis, V., Rossi, F., and Maione, S. (2005b). Molecular methods for neuropathic pain treatment. J. Neuropathic Pain 1,35-42.
53. Siniscalco, D., Giordano, C., Galderisi, U., Luongo, L., Alessio, N., Di Bernardo, G., de Novellis, V., Rossi, F., and Maione, S. (2010). Intra-brainmicroinjectionof humanmes-enchymal stem cells decreases allo-dyniainneuropathicmice. Cell. Mol. Life Sci. 67, 655-669.
54. Siniscalco, D., Rossi, F., and Maione, S. (2007). Molecular approaches for neuropathic pain treatment. Curr. Med. Chem. 14, 1783-1787.
55. Siniscalco, D., Rossi, F., and Maione, S. (2008). Stem cell therapy for neuro-pathic pain treatment. J. Stem Cells Regen. Med. 3, 2-11.
56. Sze, S. K., de Kleijn, D. P., Lai, R. C., Tan, E. K., Zhao, H., Yeo, K. S., Low, T. Y., Lian, Q., Lee, C. N., Mitchell, W., El Oakley, R. M., and Lim, S. K. (2007). Elucidating the secretion proteomeof humanembryonicstem cell-derivedmesenchymalstemcells. Mol. Cell Proteomics 6, 1680-1689.
57. Vallejo, R., Tilley, D. M., Vogel, L., and Benyamin, R. (2010). The role of glia and the immune system in the devel-opment and maintenance of neuro-pathic pain. Pain Pract. 10, 167-184.
58. Vega-Avelaira, D., Géranton, S., and Fitzgerald, M. (2009). Differential regulation of immune responses and macrophage/neuron interactions in the dorsal root ganglion in young andadultratsfollowingnerveinjury. Mol. Pain 5, 70.
59. Wang, Z., Wang, J., Li, X., Yuan, Y., and Fan, G. (2008). Interleukin-1 beta of Red nucleus involved in the development of allodynia in spared nerveinjuryrats. Exp. Brain Res.188, 379-384.
60. Zenonos, G., and Kim, J. E. (2010). A T cell-orchestrated immune response in the adult dorsal spinal cord as a cause of neuropathic pain-like hypersensitivity after periph-eral nerve damage: a door to novel therapies? Neurosurgery 66, N24-N25.
61. Zhuo, M. (2007). Neuronal mechanism forneuropathicpain. Mol. Pain 3,14.
62. Zuk, P. A., Zhu, M., Ashjian, P., De Ugarte, D. A., Huang, J. I., Mizuno, H., Alfonso, Z. C., Fraser, J. K., Ben-haim, P., and Hedrick, M. H. (2002). Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell 13, 4279-4295.