Monocytes are essential for the neuroprotective effect of human cord blood cells following middle cerebral artery occlusion in rat

Molecular and Cellular Neuroscience

Volumn 59, Issue , 2014, Pages 76-84

  Womble, T A ^a,b   Green, S ^a,b   Shahaduzzaman, M ^a,b   Grieco, J ^a   Sanberg, P R ^a,b   Pennypacker, K R ^a   Willing, A E ^a,b  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Behavior; Cerebral ischemia; Cord blood; Infarct; Microglia; Monocytes

Indexed keywords

CD133 ANTIGEN; CD14 ANTIGEN; CD19 ANTIGEN; CD2 ANTIGEN; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; PEPTIDE;

ANIMAL; B LYMPHOCYTE; CYTOLOGY; FETUS BLOOD; GENETICS; HEMATOPOIETIC STEM CELL; HUMAN; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; METABOLISM; MONOCYTE; RAT; SPRAGUE DAWLEY RAT; T LYMPHOCYTE; TRANSPLANTATION;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD14; ANTIGENS, CD19; ANTIGENS, CD2; B-LYMPHOCYTES; FETAL BLOOD; GLYCOPROTEINS; HEMATOPOIETIC STEM CELLS; HUMANS; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MONOCYTES; PEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; T-LYMPHOCYTES;

EID: 84894084750     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2014.01.004     Document Type: Article

References (53)

1. Auffray C., Sieweke M.H., Geissmann F. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 2009, 27:669-692.
2. Awad O., Dedkov E.I., Jiao C., Bloomer S., Tomanek R.J., Schatteman G.C. Differential healing activities of CD34+ and CD14+ endothelial cell progenitors. Arterioscler. Thromb. Vasc. Biol. 2006, 26:758-764.
3. Block F., Schwarz M. Dextromethorphan reduces functional deficits and neuronal damage after global ischemia in rats. Brain Res. 1996, 741:153-159.
4. Boltze J., Kowalski I., Förschler A., Schmidt U., Wagner D., Lobsien D., Emmrich J., Egger D., Kamprad M., Blunk J., Emmrich F. The stairway: a novel behavioral test detecting sensomotoric stroke deficits in rats. Artificial Organs 2006, 30:756-763.
5. + and CD34 cord blood cells. Ger. Med. Sci. 2008, 3. (Doc 9).
6. Boltze J., Schmidt U.R., Reich D.M., Kranz A., Reymann K.G., Strassburger M., Lobsien D., Wagner D.C., Forschler A., Schabitz W.R. Determination of the therapeutic time window for human umbilical cord blood mononuclear cell transplantation following experimental stroke in rats. Cell Transplant. 2012, 21:1199-1211.
7. Boltze J., Reich D.M., Hau S., Reymann K.G., Strassburger M., Lobsein D., Wagner D.-C., Kamprad M., Stahl T. Assessment of neuroprotective effects of human umbilical cord blood mononuclear cell subpopulations in vitro and in vivo. Cell Transplant. 2012, 21:723-737.
8. Borlongan C.V., Cahill D.W., Sanberg P.R. Locomotor and passive avoidance deficits following occlusion of the middle cerebral artery. Physiol. Behav. 1995, 58:909-917.
9. Borlongan C.V., Martinez R., Shytle R.D., Freeman T.B., Cahill D.W., Sanberg P.R. Striatal dopamine-mediated motor behavior is altered following occlusion of the middle cerebral artery. Pharmacol. Biochem. Behav. 1995, 52:225-229.
10. Borlongan C.V., Hadman M., Davis Sanberg C., Sanberg P.R. CNS entry of peripherally injected umbilical cord blood cells is not required for neuroprotection in stroke. Stroke 2004, 35:2385-2389.
11. Brichard B., Varis I., Latinne D., Deneys V., de Bruyere M., Leveugle P., Cornu G. Intracellular cytokine profile of cord and adult blood monocytes. Bone Marrow Transplant. 2001, 27:1081-1086.
12. Chen J., Sanberg P.R., Li Y., Wang L., Lu M., Willing A.E., Sanchez-Ramos J., Chopp M. Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats. Stroke 2001, 32:2682-2688.
13. Filias A., Theodorou G., Mouzopoulou S., Varvarigou A., Mantagos S., Karakantza M. Phagocytic ability of neutrophils and monocytes in neonates. BMC Pediatr. 2011, 11:29.
14. Geissmann F., Auffray C., Palframan R., Wirrig C., Ciocca A., Campisi L., Narni-Mancinelli E., Lauvau G. Blood monocytes: distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses. Immunol. Cell Biol. 2008, 86:398-408.
15. Gemma C., Catlow B., Cole M., Hudson C., Samec A., Shah N., Vila J., Bachstetter A., Bickford P.C. Early inhibition of TNFalpha increases 6-hydroxydopamine-induced striatal degeneration. Brain Res. 2007, 1147:240-247.
16. Gille C., Leiber A., Mundle I., Spring B., Abele H., Spellerberg B., Hartmann H., Poets C.F., Orlikowsky T.W. Phagocytosis and postphagocytic reaction of cord blood and adult blood monocyte after infection with green fluorescent protein-labeled Escherichia coli and Group B Streptococci. Cytometry B 2009, 76B:271-284.
17. Golden J.E., Shahaduzzaman M., Wabnitz A., Green S., Womble T.A., Sanberg P.R., Pennypacker K.R., Willing A.E. Human umbilical cord blood cells alter blood and spleen cell populations after stroke. Transl. Stroke Res. 2012, 3:491-499.
18. Hall A.A., Leonardo C.C., Collier L.A., Rowe D.D., Willing A.E., Pennypacker K.R. Delayed treatments for stroke influence neuronal death in rat organotypic slice cultures subjected to oxygen glucose deprivation. Neurosci. 2009, 164:470-477.
19. Hossne J.N.A., Invitti A.L., Buffolo E., Azevedo S., de Oliveira J.S.R., Stolf N.G., Cruz L.E., Sanberg P.R. Refractory angina cell therapy (ReACT) involving autologous bone marrow cells in patients without left ventricular dysfunction: a possible role for monocytes. Cell Transplant. 2009, 18:1299-1310.
20. Jiang Q., Azuma E., Hirayama M., Iwamoto S., Kumamoto T., Kobayashi M., Yamamoto H., Sakurai M., Komada Y. Functional immaturity of cord blood monocytes as detected by impaired response to hepatocyte growth factor. Ped. Intl. 2001, 43:334-339.
21. Jiang L., Womble T., Saporta S., Chen N., Sanberg C.D., Sanberg P.R., Willing A.E. Human umbilical cord blood cells depress the microglial inflammatory response in vitro. Stem Cells Dev. 2010, 19:221-227.
22. Kern D.S., Maclean K.N., Jiang H., Synder E.Y., Sladek J.R., Bjugstad K.B. Neural stem cells reduce hippocampal tau and reelin accumulation in aged Ts65Dn Down Syndrome mice. Cell Transplant. 2011, 20:371-379.
23. Kondziolka D., Wechsler L., Goldstein S., Meltzer C., Thulborn K.R., Gebel J., Jannetta P., DeCesare S., Elder E.M., McGrogan M., Reitman M.A., Bynum L. Transplantation of cultured human neuronal cells for patients with stroke. Neurology 2000, 55:565-569.
24. Kozłowska H., Jabłonka J., Janowski M., Jurga M., Kossut M., Domańska-Janik K. Transplantation of a novel human cord blood-derived neural-like stem cell line in a rat model of cortical infarct. Stem Cells Dev. 2007, 16:481-488.
25. Kriz J. Inflammation in ischemic brain injury: timing is important. Crit. Rev. Neurobiol. 2006, 18:145-157.
26. Lalancette-Hebert M., Gowing G., Simard A., Weng Y.C., Kriz J. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neurosci. 2007, 27:2596-2605.
27. Le T., Leung L., Carroll W.L., Schibler K.R. Regulation of interleukin-10 gene expression: possible mechanisms accounting for its upregulation and for maturational differences in its expression by blood mononuclear cells. Blood 1997, 89:4112-4119.
28. Leonardo C., Hall A.A., Collier L.A., Ajmo C.T., Willing A.E., Pennypacker K.R. HUCB cell therapy blocks the morphological change and recruitment of CD11b-expressing, isolectin-binding proinflammatory cells after MCAO. J. Neurosci. Res. 2010, 88:1213-1222.
29. Liu E., Tu W., Law H.K.W., Lau Y.-L. Decreased yield, phenotypic expression and function of immature monocyte-derived dendritic cells in cord blood. Br. J. Haematol. 2001, 113:240-246.
30. Liu H.-Y., Zhang Q.-J., Li H.-J., Han Z.-C. Effect of intracranial transplantation of CD34+ cells derived from human umbilical cord blood in rats with cerebral ischemia. Chin. Med. J. 2006, 119:1744-1748.
31. Mampalam T.J., Gonzalez M.F., Weinstein P., Sharp F.R. Neuronal changes in fetal cortex transplanted to ischemic adult rat cortex. J. Neurosurg. 1988, 69:904-912.
32. Marchetti V., Yanes O., Aguilar E., Wang M., Friedlander D., Moreno S., Storm K., Zhan M., Naccache S., Nemerow G., Siuzdak G., Friedlander M. Differential macrophage polarization promotes tissue remodeling and repair in a model of ischemic retinopathy. Sci. Rep. 2011, 1.
33. McDonald J.H. Handbook of Biological Statistics 2009, Sparky House Publishing, Baltimore, Maryland. 2nd ed.
34. Newcomb J.D., Ajmo C.T., Davis Sanberg C., Sanberg P.R., Pennypacker K.R., Willing A.E. Timing of cord blood treatment after experimental stroke determines therapeutic efficacy. Cell Transplant. 2006, 15:213-223.
35. Poignet H., Beaughard M., Lecoin G., Massingham R. Functional, behavioral, and histological changes induced by transient global cerebral ischemia in rats: effects of cinnarizine and flunarizine. J. Cereb. Blood Flow Metab. 1989, 9:646-654.
36. Puurunen K., Sirvio J., Koistinaho J., Miettinen R., Haapalinna A., Riekkinen P., Sivenius J. Studies on the influence of enriched-environment housing combined with systemic administration of an {alpha}2-adrenergic antagonist on spatial learning and hyperactivity after global ischemia in rats. Stroke 1997, 28:623-631.
37. Randolph G.J., Jakubzick C., Qu C. Antigen presentation by monocytes and monocyte-derived cells. Curr. Opin. Immunol. 2008, 20:52-60.
38. Roger V.L., Go A.S., Lloyd-Jones D.M., Adams R.J., Berry J.D., Brown T.M., Carnethon M.R., Dai S., de Simone G., Ford E.S., Fox C.S., Fullerton H.J., Gillespie C., Greenlund K.J., Hailpern S.M., Heit J.A., Ho P.M., Howard V.J., Kissela B.M., Kittner S.J., Lackland D.T., Lichtman J.H., Lisabeth L.D., Makuc D.M., Marcus G.M., Marelli A., Matchar D.B., McDermott M.M., Meigs J.B., Moy C.S., Mozaffarian D., Mussolino M.E., Nichol G., Paynter N.P., Rosamond W.D., Sorlie P.D., Stafford R.S., Turan T.N., Turner M.B., Wong N.D., Wylie-Rosett J. Heart disease and stroke statistics - 2011 update: a report from the American Heart Association. Circulation 2011, 123:e1-e192. on behalf of the American Heart Association Statistics Committee and Stroke Statistics Subcommittee.
39. Sanberg P.R., Zoloty S.A., Willis R., Ticarich C.D., Rhoads K., Nagy R.P., Mitchell S.G., Laforest A.R., Jenks J.A., Harkabus L.J. Digiscan activity: automated measurement of thigmotactic and stereotypic behavior in rats. Pharmacol. Biochem. Behav. 1987, 27:569-572.
40. Sanberg P.R., Park D.-H., Kuzmin-Nichols N., Cruz E., Hossne J.N.A., Buffolo E., Willing A.E. Monocyte transplantation for neural and cardiovascular ischemia repair. J. Cell. Mol. Med. 2010, 14:553-563.
41. + cells and monocytes provide significant improvement for hindlimb ischemia, although they do not transdifferentiate into endothelial cells. Cell Transplant. 2010, 19:103-112.
42. Sladek J.R., Bjugstad K.B. The future of stem cell applications: charting the sea of opportunity. Technol. Innov. 2011, 13:63-74.
43. Slaney C.Y., Toker A., La Flamme A., Backstrom B.T., Harper J.L. Naive blood monocytes suppress T-cell function. A possible mechanism for protection from autoimmunity. Immunol. Cell Biol. 2011, 89:7-13.
44. Smirkin A., Matsumoto H., Takahashi H., Inoue A., Tagawa M., Ohue S., Watanabe H., Yano H., Kumon Y., Ohnishi T., Tanaka J. Iba1+/NG2+ macrophage-like cells expressing a variety of neuroprotective factors ameliorate ischemic damage of the brain. J. Cereb. Blood Flow Metab. 2010, 30:603-615.
45. Taguchi A., Soma T., Tanaka H., Kanda T., Nishimura H., Yoshikawa H., Tsukamoto Y., Iso H., Fujimori Y., Stern D.M., Naritomi H., Matsuyama T. Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J. Clin. Invest. 2004, 114:330-338.
46. Tonder N., Sorensen T., Zimmer J., Jorgensen M.B., Johansen F.F., Diemer N.H. Neural grafting to ischemic lesions of the adult rat hippocampus. Exp. Brain Res. 1989, 74:512-526.
47. Van Voorhis W.C., Valinsky J., Hoffman E., Luban J., Hair L.S., Steinman R.M. Relative efficacy of human monocytes and dendritic cells as accessory cells for T cell replication. J. Exp. Med. 1983, 158:174-191.
48. Vendrame M., Cassady C.J., Newcomb J., Butler T., Pennypacker K.R., Zigova T., Davis Sanberg C., Sanberg P.R., Willing A.E. Infusion of human umbilical cord blood cells in a rat model of stroke dose-dependently rescues behavioral deficits and reduces infarct volume. Stroke 2004, 35:2390-2395.
49. Vendrame M., Gemma C., de Mesquita D., Collier L., Bickford P.C., Davis Sanberg C., Sanberg P.R., Pennypacker K.R., Willing A.E. Anti-inflammatory effects of human cord blood cells in a rat model of stroke. Stem Cells Dev. 2005, 14:595-604.
50. Willing A.E., Nowicki P., Poulos S., Lixian J., Milliken M., Cahill D.W., Sanberg P.R. Effects of middle cerebral artery occlusion on spontaneous activity and cognitive function in rats. Int. J. Neurosci. 2002, 112:503-516.
51. Willing A.E., Lixian J., Milliken M., Poulos S., Zigova T., Song S., Hart C., Sanchez-Ramos J., Sanberg P.R. Intravenous versus intrastriatal cord blood administration in a rodent model of stroke. J. Neurosci. Res. 2003, 73:296-307.
52. Xiao J., Nan Z., Motooka Y., Low W.C. Transplantation of a novel cell line population of umbilical cord blood stem cells ameliorates neurological deficits associated with ischemic brain injury. Stem Cells Dev. 2005, 14:722-733.
53. Yang M., Wei X., Li J., Heine L.A., Rosenwasser R., Iacovitti L. Changes in host blood factors and brain glia accompanying the functional recovery after systemic administration of bone marrow stem cells in ischemic stroke rats. Cell Transplant. 2010, 19:1073-1084.