Human umbilical cord blood cells protect oligodendrocytes from brain ischemia through Akt signal transduction

Journal of Biological Chemistry

Volumn 287, Issue 6, 2012, Pages 4177-4187

  Rowe, Derrick D ^a   Leonardo, Christopher C ^b   Recio, Jesus A ^a   Collier, Lisa A ^a   Willing, Alison E ^a   Pennypacker, Keith R ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4-LEVEL; AKT PHOSPHORYLATION; BRAIN ISCHEMIA; CASPASE-3; HUMAN UMBILICAL CORD; IN-VITRO; IN-VIVO; ISCHEMIC CONDITIONS; ISCHEMIC INJURIES; MIDDLE CEREBRAL ARTERY; OLIGODENDROCYTES; OXYGEN GLUCOSE DEPRIVATION; PROTECTIVE EFFECTS; PROTEIN EXPRESSIONS; PROTEOLYTIC CLEAVAGE; SYSTEMIC ADMINISTRATION; WHITE MATTER;

BLOOD VESSELS; CELL CULTURE; CELLS; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

BLOOD;

CASPASE 3; PEROXIREDOXIN 4; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CELL; BRAIN DAMAGE; BRAIN DEGENERATION; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; GLIA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; UMBILICAL CORD BLOOD CELL; WHITE MATTER;

ANIMALS; BRAIN ISCHEMIA; CASPASE 3; CELL SURVIVAL; HUMANS; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; PEROXIREDOXINS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; UMBILICAL CORD;

EID: 84856726620     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.296434     Document Type: Article

References (52)

1. Vendrame, M., Cassady, J., Newcomb, J., Butler, T., Pennypacker, K. R., Zigova, T., Sanberg, C. D., Sanberg, P. R., and Willing, A. E. (2004) Infusion of human umbilical cord blood cells in a rat model of stroke dose-dependently rescues behavioral deficits and reduces infarct volume. Stroke 35, 2390-2395 (Pubitemid 39311269)
2. Newman, M. B., Willing, A. E., Manresa, J. J., Davis-Sanberg, C., and Sanberg, P. R. (2005) Stroke-induced migration of human umbilical cord blood cells. Time course and cytokines. Stem Cells Dev. 14, 576-586 (Pubitemid 41780809)
3. Hall, A. A., Guyer, A. G., Leonardo, C. C., Ajmo, C. T., Jr., Collier, L. A., Willing, A. E., and Pennypacker, K. R. (2009) Human umbilical cord blood cells directly suppress ischemic oligodendrocyte cell death. J. Neurosci. Res. 87, 333-341
4. Nieda, M., Nicol, A., Denning-Kendall, P., Sweetenham, J., Bradley, B., and Hows, J. (1997) Endothelial cell precursors are normal components of human umbilical cord blood. Br. J. Haematol. 98, 775-777 (Pubitemid 27386564)
5. Erices, A., Conget, P., and Minguell, J. J. (2000) Mesenchymal progenitor cells in human umbilical cord blood. Br. J. Haematol. 109, 235-242 (Pubitemid 30340601)
6. Nakahata, T., and Ogawa, M. (1982) Hemopoietic colony-forming cells in umbilical cord blood with extensive capability to generate mono- and multipotential hemopoietic progenitors. J. Clin. Invest. 70, 1324-1328 (Pubitemid 13168016)
7. Kulik, G., Klippel, A., and Weber, M. J. (1997) Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphatidylinositol 3-kinase, and Akt. Mol. Cell. Biol. 17, 1595-1606 (Pubitemid 27097389)
8. Jin, K. L., Mao, X. O., and Greenberg, D. A. (2000) Vascular endothelial growth factor. Direct neuroprotective effect in in vitro ischemia. Proc. Natl. Acad. Sci. U.S.A. 97, 10242-10247
9. Neuhoff, S., Moers, J., Rieks, M., Grunwald, T., Jensen, A., Dermietzel, R., and Meier, C. (2007) Proliferation, differentiation, and cytokine secretion of human umbilical cord blood-derived mononuclear cells in vitro. Exp. Hematol. 35, 1119-1131 (Pubitemid 46921308)
10. Newman, M. B., Willing, A. E., Manresa, J. J., Sanberg, C. D., and Sanberg, P. R. (2006) Cytokines produced by cultured human umbilical cord blood (HUCB) cells. Implications for brain repair. Exp. Neurol. 199, 201-208
11. Mullonkal, C. J., and Toledo-Pereyra, L. H. (2007) Akt in ischemia and reperfusion. J. Invest. Surg. 20, 195-203 (Pubitemid 47050383)
12. Zhao, Y., Patzer, A., Herdegen, T., Gohlke, P., and Culman, J. (2006) Activation of cerebral peroxisome proliferator-activated receptors gamma promotes neuroprotection by attenuation of neuronal cyclooxygenase-2 overexpression after focal cerebral ischemia in rats. FASEB J. 20, 1162-1175 (Pubitemid 44943912)
13. Dasari, V. R., Veeravalli, K. K., Saving, K. L., Gujrati, M., Fassett, D., Klopfenstein, J. D., Dinh, D. H., and Rao, J. S. (2008) Neuroprotection by cord blood stem cells against glutamate-induced apoptosis is mediated by Akt pathway. Neurobiol. Dis. 32, 486-498
14. Rowe, D. D., Leonardo, C. C., Hall, A. A., Shahaduzzaman, M. D., Collier, L. A., Willing, A. E., and Pennypacker, K. R. (2010) Cord blood administration induces oligodendrocyte survival through alterations in gene expression. Brain Res. 1366, 172-188
15. McCarthy, K. D., and de Vellis, J. (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85, 890-902 (Pubitemid 10007455)
16. Butler, T. L., Kassed, C. A., Sanberg, P. R., Willing, A. E., and Pennypacker, K. R. (2002) Neurodegeneration in the rat hippocampus and striatum after middle cerebral artery occlusion. Brain Res. 929, 252-260 (Pubitemid 34178341)
17. Leonardo, C. C., Hall, A. A., Collier, L. A., Ajmo, C. T., Jr., Willing, A. E., and Pennypacker, K. R. (2010) Human umbilical cord blood cell therapy blocks the morphological change and recruitment of CD11b-expressing, isolectin-binding proinflammatory cells after middle cerebral artery occlusion. J. Neurosci. Res. 88, 1213-1222
18. Kau, T. R., Schroeder, F., Ramaswamy, S., Wojciechowski, C. L., Zhao, J. J., Roberts, T. M., Clardy, J., Sellers, W. R., and Silver, P. A. (2003)Achemical genetic screen identifies inhibitors of regulated nuclear export of a Forkhead transcription factor in PTEN-deficient tumor cells. Cancer Cell 4, 463-476 (Pubitemid 38050043)
19. Zhao, H., Sapolsky, R. M., and Steinberg, G. K. (2006) Phosphoinositide-3-kinase/akt survival signal pathways are implicated in neuronal survival after stroke. Mol. Neurobiol. 34, 249-270
20. Okado-Matsumoto, A., Matsumoto, A., Fujii, J., and Taniguchi, N. (2000) Peroxiredoxin IV is a secretable protein with heparin-binding properties under reduced conditions. J. Biochem. 127, 493-501 (Pubitemid 30185255)
21. Brouns, R., De Vil, B., Cras, P., De Surgeloose, D., Mariën, P., and De Deyn, P. P. (2010) Neurobiochemical markers of brain damage in cerebrospinal fluid of acute ischemic stroke patients. Clin. Chem. 56, 451-458
22. Lyons, S. A., and Kettenmann, H. (1998) Oligodendrocytes and microglia are selectively vulnerable to combined hypoxia and hypoglycemia injury in vitro. J. Cereb. Blood Flow Metab. 18, 521-530 (Pubitemid 28213536)
23. Pantoni, L., Garcia, J. H., and Gutierrez, J. A. (1996) Stroke 27, 1641-1646; discussion, 1647
24. McTigue, D. M., and Tripathi, R. B. (2008) The life, death, and replacement of oligodendrocytes in the adult CNS. J Neurochem. 107, 1-19
25. Lee, S. J., Yoo, H. J., Bae, Y. S., Kim, H. J., and Lee, S. T. (2003) TIMP-1 inhibits apoptosis in breast carcinoma cells via a pathway involving pertussis toxin-sensitive G protein and c-Src. Biochem. Biophys. Res. Commun. 312, 1196-1201 (Pubitemid 37490943)
26. Lentzsch, S., Chatterjee, M., Gries, M., Bommert, K., Gollasch, H., Dörken, B., and Bargou, R. C. (2004) PI3-K/AKT/FKHR and MAPK signaling cascades are redundantly stimulated by a variety of cytokines and contribute independently to proliferation and survival of multiple myeloma cells. Leukemia 18, 1883-1890 (Pubitemid 39530020)
27. Wegiel, B., Bjartell, A., Culig, Z., and Persson, J. L. (2008) Interleukin-6 activates PI3K/Akt pathway and regulates cyclin A1 to promote prostate cancer cell survival. Int. J. Cancer 122, 1521-1529 (Pubitemid 351294960)
28. Dolcet, X., Egea, J., Soler, R. M., Martin-Zanca, D., and Comella, J. X. (1999) Activation of phosphatidylinositol 3-kinase, but not extracellular- regulated kinases, is necessary to mediate brain-derived neurotrophic factor-induced motoneuron survival. J. Neurochem. 73, 521-531 (Pubitemid 29339824)
29. Shibata, M., Yamawaki, T., Sasaki, T., Hattori, H., Hamada, J., Fukuuchi, Y., Okano, H., and Miura, M. (2002) Upregulation of Akt phosphorylation at the early stage of middle cerebral artery occlusion in mice. Brain Res. 942, 1-10 (Pubitemid 34597063)
30. Noshita, N., Lewén, A., Sugawara, T., and Chan, P. H. (2001) Evidence of phosphorylation of Akt and neuronal survival after transient focal cerebral ischemia in mice. J. Cereb. Blood Flow Metab. 21, 1442-1450 (Pubitemid 33120944)
31. Datta, S. R., Brunet, A., and Greenberg, M. E. (1999) Cellular survival. A play in three Akts. Genes Dev. 13, 2905-2927
32. Le Rhun, Y., Kirkland, J. B., and Shah, G. M. (1998) Cellular responses to DNA damage in the absence of poly(ADP-ribose) polymerase. Biochem. Biophys. Res. Commun. 245, 1-10 (Pubitemid 28414236)
33. Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., and Lazebnik, Y. A. (1995) Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376, 37-43
34. Hall, A., Sankaran, B., Poole, L. B., and Karplus, P. A. (2009) Structural changes common to catalysis in the Tpx peroxiredoxin subfamily. J. Mol. Biol. 393, 867-881
35. Ho, J. N., Lee, S. B., Lee, S. S., Yoon, S. H., Kang, G. Y., Hwang, S. G., and Um, H. D. (2010) Phospholipase A2 activity of peroxiredoxin 6 promotes invasion and metastasis of lung cancer cells. Mol. Cancer Ther. 9, 825-832
36. Haridas, V., Ni, J., Meager, A., Su, J., Yu, G. L., Zhai, Y., Kyaw, H., Akama, K. T., Hu, J., Van Eldik, L. J., and Aggarwal, B. B. (1998) TRANK, a novel cytokine that activates NF-kappa B and c-Jun N-terminal kinase. J. Immunol. 161, 1-6 (Pubitemid 28285498)
37. Carnero, A., Blanco-Aparicio, C., Renner, O., Link, W., and Leal, J. F. (2008) The PTEN/PI3K/AKT signalling pathway in cancer, therapeutic implications. Curr. Cancer Drug Targets 8, 187-198 (Pubitemid 351688437)
38. Kwon, J., Lee, S. R., Yang, K. S., Ahn, Y., Kim, Y. J., Stadtman, E. R., and Rhee, S. G. (2004) Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc. Natl. Acad. Sci. U.S.A. 101, 16419-16424 (Pubitemid 39557728)
39. Radyuk, S. N., Michalak, K., Klichko, V. I., Benes, J., and Orr, W. C. (2010) Peroxiredoxin 5 modulates immune response in Drosophila. Biochim. Biophys. Acta 1800, 1153-1163
40. Jung, H., Kim, T., Chae, H. Z., Kim, K. T., and Ha, H. (2001) Regulation of macrophage migration inhibitory factor and thiol-specific antioxidant protein PAG by direct interaction. J. Biol. Chem. 276, 15504-15510
41. Hwang, I. K., Yoo, K. Y., Kim, D. W., Lee, C. H., Choi, J. H., Kwon, Y. G., Kim, Y. M., Choi, S. Y., and Won, M. H. (2010) Changes in the expression of mitochondrial peroxiredoxin and thioredoxin in neurons and glia and their protective effects in experimental cerebral ischemic damage. Free Radic. Biol. Med. 48, 1242-1251
42. Plaisant, F., Clippe, A., Vander Stricht, D., Knoops, B., and Gressens, P. (2003) Recombinant peroxiredoxin 5 protects against excitotoxic brain lesions in newborn mice. Free Radic. Biol. Med. 34, 862-872 (Pubitemid 36316071)
43. Hofmann, B., Hecht, H. J., and Flohé, L. (2002) Peroxiredoxins. Biol. Chem. 383, 347-364 (Pubitemid 34506276)
44. Jang, H. H., Lee, K. O., Chi, Y. H., Jung, B. G., Park, S. K., Park, J. H., Lee, J. R., Lee, S. S., Moon, J. C., Yun, J. W., Choi, Y. O., Kim, W. Y., Kang, J. S., Cheong, G. W., Yun, D. J., Rhee, S. G., Cho, M. J., and Lee, S. Y. (2004) Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117, 625-635 (Pubitemid 38692528)
45. Kang, S. W., Rhee, S. G., Chang, T. S., Jeong, W., and Choi, M. H. (2005) 2-Cys peroxiredoxin function in intracellular signal transduction: therapeutic implications. Trends Mol. Med. 11, 571-578 (Pubitemid 41713999)
46. Jin, M. H., Lee, Y. H., Kim, J. M., Sun, H. N., Moon, E. Y., Shong, M. H., Kim, S. U., Lee, S. H., Lee, T. H., Yu, D. Y., and Lee, D. S. (2005) Characterization of neural cell types expressing peroxiredoxins in mouse brain. Neurosci. Lett. 381, 252-257 (Pubitemid 40719167)
47. Kassed, C. A., Willing, A. E., Garbuzova-Davis, S., Sanberg, P. R., and Pennypacker, K. R. (2002) Lack of NF-kappaB p50 exacerbates degeneration of hippocampal neurons after chemical exposure and impairs learning. Exp. Neurol. 176, 277-288 (Pubitemid 35193345)
48. Fridmacher, V., Kaltschmidt, B., Goudeau, B., Ndiaye, D., Rossi, F. M., Pfeiffer, J., Kaltschmidt, C., Israël, A., and Mémet, S. (2003) Forebrain-specific neuronal inhibition of nuclear factor-κB activity leads to loss of neuroprotection. J. Neurosci. 23, 9403-9408 (Pubitemid 37323040)
49. Won, H., Lim, S., Jang, M., Kim, Y., Rashid, M. A., Jyothi, K. R., Dashdorj, A., Kang, I., Ha, J., and Kim, S. S. (2012) Peroxiredoxin-2 up-regulated by NF-κB attenuates oxidative stress during the differentiation of muscle-derived C2C12 cells. Antioxid. Redox Signal. 16, 245-261
50. Newcomb, J. D., Ajmo, C. T., Jr., Sanberg, C. D., Sanberg, P. R., Pennypacker, K. R., and Willing, A. E. (2006) Timing of cord blood treatment after experimental stroke determines therapeutic efficacy. Cell Transplant 15, 213-223 (Pubitemid 43726180)
51. Chua, S. J., Bielecki, R., Yamanaka, N., Fehlings, M. G., Rogers, I. M., and Casper, R. F. (2010) The effect of umbilical cord blood cells on outcomes after experimental traumatic spinal cord injury. Spine 35, 1520-1526
52. Garbuzova-Davis, S., Willing, A. E., Zigova, T., Saporta, S., Justen, E. B., Lane, J. C., Hudson, J. E., Chen, N., Davis, C. D., and Sanberg, P. R. (2003) Intravenous administration of human umbilical cord blood cells in a mouse model of amyotrophic lateral sclerosis: distribution, migration, and differentiation. J. Hematother. Stem Cell Res. 12, 255-270 (Pubitemid 36736737)