Induction of neuro-protective/regenerative genes in stem cells infiltrating post-ischemic brain tissue

Experimental and Translational Stroke Medicine

Volumn 2, Issue 1, 2010, Pages

  Yilmaz, Gokhan ^a   Alexander, J Steven ^a   Erkuran Yilmaz, Cigdem ^b   Granger, D Neil ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b CITY UNIVERSITY OF NEW YORK MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ISCHEMIA; BRAIN TISSUE; CELL DIFFERENTIATION; CELL REGENERATION; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; EPIGENETICS; GENE EXPRESSION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; MALE; MICROARRAY ANALYSIS; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REPERFUSION; STROKE; STROMA CELL; TREATMENT OUTCOME;

EID: 78650657561     PISSN: None     EISSN: 20407378     Source Type: Journal    
DOI: 10.1186/2040-7378-2-11     Document Type: Article

References (67)

1. Chopp M, Li Y. Treatment of neural injury with marrow stromal cells. Lancet Neurol 2002, 1:92-100. 10.1016/S1474-4422(02)00040-6, 12849513.
2. Zhang J, Li Y, Chen J, Cui Y, Lu M, Elias SB, Mitchell JB, Hammill L, Vanguri P, Chopp M. Human bone marrow stromal cell treatment improves neurological functional recovery in EAE mice. Exp Neurol 2005, 195:16-26. 10.1016/j.expneurol.2005.03.018, 15904921.
3. Chen J, Li Y, Wang L, Zhang Z, Lu D, Lu M, Chopp M. Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 2001, 32:1005-1011.
4. Li Y, Chen J, Wang L, Lu M, Chopp M. Treatment of stroke in rat with intracarotid administration of marrow stromal cells. Neurology 2001, 56:1666-1672.
5. Chen J, Zhang ZG, Li Y, Wang L, Xu YX, Gautam SC, Lu M, Zhu Z, Chopp M. Intravenous administration of human bone marrow stromal cells induces angiogenesis in the ischemic boundary zone after stroke in rats. Circ Res 2003, 92:692-699. 10.1161/01.RES.0000063425.51108.8D, 12609969.
6. Chen J, Li Y, Katakowski M, Chen X, Wang L, Lu D, Lu M, Gautam SC, Chopp M. Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J Neurosci Res 2003, 73:778-786. 10.1002/jnr.10691, 12949903.
7. Qu R, Li Y, Gao Q, Shen L, Zhang J, Liu Z, Chen X, Chopp M. Neurotrophic and growth factor gene expression profiling of mouse bone marrow stromal cells induced by ischemic brain extracts. Neuropathology 2007, 27:355-363. 10.1111/j.1440-1789.2007.00792.x, 2593420, 17899689.
8. Bliss T, Guzman R, Daadi M, Steinberg GK. Cell transplantation therapy for stroke. Stroke 2007, 38:817-826. 10.1161/01.STR.0000247888.25985.62, 17261746.
9. Ohtaki H, Ylostalo JH, Foraker JE, Robinson AP, Reger RL, Shioda S, Prockop DJ. Stem/progenitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflammatory/immune responses. Proc Natl Acad Sci USA 2008, 105:14638-14643. 10.1073/pnas.0803670105, 2567180, 18794523.
10. Kelly S, Bliss TM, Shah AK, Sun GH, Ma M, Foo WC, Masel J, Yenari MA, Weissman IL, Uchida N, et al. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc Natl Acad Sci USA 2004, 101:11839-11844. 10.1073/pnas.0404474101, 511061, 15280535.
11. Ishibashi S, Sakaguchi M, Kuroiwa T, Yamasaki M, Kanemura Y, Shizuko I, Shimazaki T, Onodera M, Okano H, Mizusawa H. Human neural stem/progenitor cells, expanded in long-term neurosphere culture, promote functional recovery after focal ischemia in Mongolian gerbils. J Neurosci Res 2004, 78:215-223. 10.1002/jnr.20246, 15378509.
12. Pollock K, Stroemer P, Patel S, Stevanato L, Hope A, Miljan E, Dong Z, Hodges H, Price J, Sinden JD. A conditionally immortal clonal stem cell line from human cortical neuroepithelium for the treatment of ischemic stroke. Exp Neurol 2006, 199:143-155. 10.1016/j.expneurol.2005.12.011, 16464451.
13. Dennis JE, Caplan AI. Differentiation potential of conditionally immortalized mesenchymal progenitor cells from adult marrow of a H-2Kb-tsA58 transgenic mouse. J Cell Physiol 1996, 167:523-538. 10.1002/(SICI)1097-4652(199606)167:3<523::AID-JCP16>3.0.CO;2-4, 8655606.
14. Jendelova P, Herynek V, Urdzikova L, Glogarova K, Kroupova J, Andersson B, Bryja V, Burian M, Hajek M, Sykova E. Magnetic resonance tracking of transplanted bone marrow and embryonic stem cells labeled by iron oxide nanoparticles in rat brain and spinal cord. J Neurosci Res 2004, 76:232-243. 10.1002/jnr.20041, 15048921.
15. Wu J, Sun Z, Sun HS, Weisel RD, Keating A, Li ZH, Feng ZP, Li RK. Intravenously administered bone marrow cells migrate to damaged brain tissue and improve neural function in ischemic rats. Cell Transplant 2008, 16:993-1005. 10.3727/000000007783472435, 18351015.
16. Li Y, Chopp M, Chen J, Wang L, Gautam SC, Xu YX, Zhang Z. Intrastriatal transplantation of bone marrow nonhematopoietic cells improves functional recovery after stroke in adult mice. J Cereb Blood Flow Metab 2000, 20:1311-1319. 10.1097/00004647-200009000-00006, 10994853.
17. Yilmaz G, Arumugam TV, Stokes KY, Granger DN. Role of T lymphocytes and interferon-gamma in ischemic stroke. Circulation 2006, 113:2105-2112. 10.1161/CIRCULATIONAHA.105.593046, 16636173.
18. Benjamini YH, Yosef. Controlling the False Discovery Rate: a Practical and Powerful Approach to Multiple Testing. JR Statist Soc B 1995, 57:289-300.
19. Cheadle C, Vawter MP, Freed WJ, Becker KG. Analysis of microarray data using Z score transformation. J Mol Diagn 2003, 5:73-81. 1907322, 12707371.
20. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30:207-210. 10.1093/nar/30.1.207, 99122, 11752295.
21. Doniger SW, Salomonis N, Dahlquist KD, Vranizan K, Lawlor SC, Conklin BR. MAPPFinder: using Gene Ontology and GenMAPP to create a global gene-expression profile from microarray data. Genome Biol 2003, 4:R7. 10.1186/gb-2003-4-1-r7, 151291, 12540299.
22. Borlongan CV, Hadman M, Sanberg CD, Sanberg PR. Central nervous system entry of peripherally injected umbilical cord blood cells is not required for neuroprotection in stroke. Stroke 2004, 35:2385-2389. 10.1161/01.STR.0000141680.49960.d7, 15345799.
23. Li Y, Chen J, Chen XG, Wang L, Gautam SC, Xu YX, Katakowski M, Zhang LJ, Lu M, Janakiraman N, Chopp M. Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery. Neurology 2002, 59:514-523.
24. Bang OY, Lee JS, Lee PH, Lee G. Autologous mesenchymal stem cell transplantation in stroke patients. Ann Neurol 2005, 57:874-882. 10.1002/ana.20501, 15929052.
25. Shen LH, Li Y, Chen J, Zacharek A, Gao Q, Kapke A, Lu M, Raginski K, Vanguri P, Smith A, Chopp M. Therapeutic benefit of bone marrow stromal cells administered 1 month after stroke. J Cereb Blood Flow Metab 2007, 27:6-13. 10.1038/sj.jcbfm.9600311, 16596121.
26. Shen LH, Li Y, Chen J, Zhang J, Vanguri P, Borneman J, Chopp M. Intracarotid transplantation of bone marrow stromal cells increases axon-myelin remodeling after stroke. Neuroscience 2006, 137:393-399. 10.1016/j.neuroscience.2005.08.092, 16298076.
27. Zhang ZG, Zhang L, Croll SD, Chopp M. Angiopoietin-1 reduces cerebral blood vessel leakage and ischemic lesion volume after focal cerebral embolic ischemia in mice. Neuroscience 2002, 113:683-687. 10.1016/S0306-4522(02)00175-6, 12150788.
28. Bhadriraju K, Chung KH, Spurlin TA, Haynes RJ, Elliott JT, Plant AL. The relative roles of collagen adhesive receptor DDR2 activation and matrix stiffness on the downregulation of focal adhesion kinase in vascular smooth muscle cells. Biomaterials 2009, 30:6687-6694. 10.1016/j.biomaterials.2009.08.036, 19762078.
29. Christen B, Robles V, Raya M, Paramonov I, Belmonte JC. Regeneration and reprogramming compared. BMC Biol 8:5. 10.1186/1741-7007-8-5, 2826312, 20089153.
30. Marchal L, Luxardi G, Thome V, Kodjabachian L. BMP inhibition initiates neural induction via FGF signaling and Zic genes. Proc Natl Acad Sci USA 2009, 106:17437-17442. 10.1073/pnas.0906352106, 2765096, 19805078.
31. Rousseau F, Gauchat JF, McLeod JG, Chevalier S, Guillet C, Guilhot F, Cognet I, Froger J, Hahn AF, Knappskog PM, et al. Inactivation of cardiotrophin-like cytokine, a second ligand for ciliary neurotrophic factor receptor, leads to cold-induced sweating syndrome in a patient. Proc Natl Acad Sci USA 2006, 103:10068-10073. 10.1073/pnas.0509598103, 1502507, 16782820.
32. Elson GC, Graber P, Losberger C, Herren S, Gretener D, Menoud LN, Wells TN, Kosco-Vilbois MH, Gauchat JF. Cytokine-like factor-1, a novel soluble protein, shares homology with members of the cytokine type I receptor family. J Immunol 1998, 161:1371-1379.
33. Paulsen SJ, Christensen MT, Vrang N, Larsen LK. The putative neuropeptide TAFA5 is expressed in the hypothalamic paraventricular nucleus and is regulated by dehydration. Brain Res 2008, 1199:1-9. 10.1016/j.brainres.2007.12.074, 18275939.
34. Doyle KP, Yang T, Lessov NS, Ciesielski TM, Stevens SL, Simon RP, King JS, Stenzel-Poore MP. Nasal administration of osteopontin peptide mimetics confers neuroprotection in stroke. J Cereb Blood Flow Metab 2008, 28:1235-1248. 10.1038/jcbfm.2008.17, 18364727.
35. Partridge CR, Williams ES, Barhoumi R, Tadesse MG, Johnson CD, Lu KP, Meininger GA, Wilson E, Ramos KS. Novel genomic targets in oxidant-induced vascular injury. J Mol Cell Cardiol 2005, 38:983-996. 10.1016/j.yjmcc.2005.03.006, 15910882.
36. Bayless KJ, Davis GE, Meininger GA. Isolation and biological properties of osteopontin from bovine milk. Protein Expr Purif 1997, 9:309-314. 10.1006/prep.1996.0699, 9126601.
37. Yan YP, Lang BT, Vemuganti R, Dempsey RJ. Osteopontin is a mediator of the lateral migration of neuroblasts from the subventricular zone after focal cerebral ischemia. Neurochem Int 2009, 55:826-832. 10.1016/j.neuint.2009.08.007, 19686792.
38. Steele IA, Edmondson RJ, Leung HY, Davies BR. Ligands to FGF receptor 2-IIIb induce proliferation, motility, protection from cell death and cytoskeletal rearrangements in epithelial ovarian cancer cell lines. Growth Factors 2006, 24:45-53. 10.1080/08977190500361697, 16393693.
39. Sadohara T, Sugahara K, Urashima Y, Terasaki H, Lyama K. Keratinocyte growth factor prevents ischemia-induced delayed neuronal death in the hippocampal CA1 field of the gerbil brain. Neuroreport 2001, 12:71-76. 10.1097/00001756-200101220-00022, 11201095.
40. Nakaya N, Lee HS, Takada Y, Tzchori I, Tomarev SI. Zebrafish olfactomedin 1 regulates retinal axon elongation in vivo and is a modulator of Wnt signaling pathway. J Neurosci 2008, 28:7900-7910. 10.1523/JNEUROSCI.0617-08.2008, 2692209, 18667622.
41. Filmus J, Capurro M, Rast J. Glypicans. Genome Biol 2008, 9:224. 10.1186/gb-2008-9-5-224, 2441458, 18505598.
42. Mastroiacovo F, Busceti CL, Biagioni F, Moyanova SG, Meisler MH, Battaglia G, Caricasole A, Bruno V, Nicoletti F. Induction of the Wnt antagonist, Dickkopf-1, contributes to the development of neuronal death in models of brain focal ischemia. J Cereb Blood Flow Metab 2009, 29:264-276. 10.1038/jcbfm.2008.111, 18827832.
43. Krupnik VE, Sharp JD, Jiang C, Robison K, Chickering TW, Amaravadi L, Brown DE, Guyot D, Mays G, Leiby K, et al. Functional and structural diversity of the human Dickkopf gene family. Gene 1999, 238:301-313. 10.1016/S0378-1119(99)00365-0, 10570958.
44. Hsieh JC, Kodjabachian L, Rebbert ML, Rattner A, Smallwood PM, Samos CH, Nusse R, Dawid IB, Nathans J. A new secreted protein that binds to Wnt proteins and inhibits their activities. Nature 1999, 398:431-436. 10.1038/18899, 10201374.
45. Wu W, Glinka A, Delius H, Niehrs C. Mutual antagonism between dickkopf1 and dickkopf2 regulates Wnt/beta-catenin signalling. Curr Biol 2000, 10:1611-1614. 10.1016/S0960-9822(00)00868-X, 11137016.
46. Andrade DM. Genetic basis in epilepsies caused by malformations of cortical development and in those with structurally normal brain. Hum Genet 2009, 126:173-193. 10.1007/s00439-009-0702-1, 19536565.
47. Tanaka K, Arao T, Maegawa M, Matsumoto K, Kaneda H, Kudo K, Fujita Y, Yokote H, Yanagihara K, Yamada Y, et al. SRPX2 is overexpressed in gastric cancer and promotes cellular migration and adhesion. Int J Cancer 2009, 124:1072-1080. 10.1002/ijc.24065, 19065654.
48. Miljkovic-Licina M, Hammel P, Garrido-Urbani S, Bradfield PF, Szepetowski P, Imhof BA. Sushi repeat protein X-linked 2, a novel mediator of angiogenesis. FASEB J 2009, 23:4105-4116. 10.1096/fj.09-135202, 19667118.
49. Matsuzaki K, Inoue H, Kumagai N. Re-epithelialisation and the possible involvement of the transcription factor, basonuclin. Int Wound J 2004, 1:135-140. 10.1111/j.1742-4801.2004.00033.x, 16722885.
50. Michibata H, Okuno T, Konishi N, Kyono K, Wakimoto K, Aoki K, Kondo Y, Takata K, Kitamura Y, Taniguchi T. Human GPM6A is associated with differentiation and neuronal migration of neurons derived from human embryonic stem cells. Stem Cells Dev 2009, 18:629-639. 10.1089/scd.2008.0215, 19298174.
51. Pulvers JN, Huttner WB. Brca1 is required for embryonic development of the mouse cerebral cortex to normal size by preventing apoptosis of early neural progenitors. Development 2009, 136:1859-1868. 10.1242/dev.033498, 19403657.
52. Evans TA, Raina AK, Delacourte A, Aprelikova O, Lee HG, Zhu X, Perry G, Smith MA. BRCA1 may modulate neuronal cell cycle re-entry in Alzheimer disease. Int J Med Sci 2007, 4:140-145. 1868658, 17505559.
53. Nikolova-Karakashian M, Karakashian A, Rutkute K. Role of neutral sphingomyelinases in aging and inflammation. Subcell Biochem 2008, 49:469-486. full_text, 18751923.
54. Berditchevski F. Complexes of tetraspanins with integrins: more than meets the eye. J Cell Sci 2001, 114:4143-4151.
55. Okumura K, Nogami M, Taguchi H, Dean FB, Chen M, Pan ZQ, Hurwitz J, Shiratori A, Murakami Y, Ozawa K, et al. Assignment of the 36.5-kDa (RFC5), 37-kDa (RFC4), 38-kDa (RFC3), and 40-kDa (RFC2) subunit genes of human replication factor C to chromosome bands 12q24.2-q24.3, 3q27, 13q12.3-q13, and 7q11.23. Genomics 1995, 25:274-278. 10.1016/0888-7543(95)80135-9, 7774928.
56. Yiu G, He Z. Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 2006, 7:617-627. 10.1038/nrn1956, 2693386, 16858390.
57. Liu Z, Li Y, Qu R, Shen L, Gao Q, Zhang X, Lu M, Savant-Bhonsale S, Borneman J, Chopp M. Axonal sprouting into the denervated spinal cord and synaptic and postsynaptic protein expression in the spinal cord after transplantation of bone marrow stromal cell in stroke rats. Brain Res 2007, 1149:172-180. 10.1016/j.brainres.2007.02.047, 1950288, 17362881.
58. Shen LH, Li Y, Gao Q, Savant-Bhonsale S, Chopp M. Down-regulation of neurocan expression in reactive astrocytes promotes axonal regeneration and facilitates the neurorestorative effects of bone marrow stromal cells in the ischemic rat brain. Glia 2008, 56:1747-1754. 10.1002/glia.20722, 2575136, 18618668.
59. Bartholomew A, Sturgeon C, Siatskas M, Ferrer K, McIntosh K, Patil S, Hardy W, Devine S, Ucker D, Deans R, et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 2002, 30:42-48. 10.1016/S0301-472X(01)00769-X, 11823036.
60. Djouad F, Plence P, Bony C, Tropel P, Apparailly F, Sany J, Noel D, Jorgensen C. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 2003, 102:3837-3844. 10.1182/blood-2003-04-1193, 12881305.
61. Le Blanc K, Rasmusson I, Sundberg B, Gotherstrom C, Hassan M, Uzunel M, Ringden O. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004, 363:1439-1441. 10.1016/S0140-6736(04)16104-7, 15121408.
62. Ishii M, Koike C, Igarashi A, Yamanaka K, Pan H, Higashi Y, Kawaguchi H, Sugiyama M, Kamata N, Iwata T, et al. Molecular markers distinguish bone marrow mesenchymal stem cells from fibroblasts. Biochem Biophys Res Commun 2005, 332:297-303. 10.1016/j.bbrc.2005.04.118, 15896330.
63. Foerch C, Singer OC, Neumann-Haefelin T, du Mesnil de Rochemont R, Steinmetz H, Sitzer M. Evaluation of serum S100B as a surrogate marker for long-term outcome and infarct volume in acute middle cerebral artery infarction. Arch Neurol 2005, 62:1130-1134. 10.1001/archneur.62.7.1130, 16009772.
64. Liauw J, Hoang S, Choi M, Eroglu C, Sun GH, Percy M, Wildman-Tobriner B, Bliss T, Guzman RG, Barres BA, Steinberg GK. Thrombospondins 1 and 2 are necessary for synaptic plasticity and functional recovery after stroke. J Cereb Blood Flow Metab 2008, 28:1722-1732. 10.1038/jcbfm.2008.65, 18594557.
65. Russell JC, Szuflita N, Khatri R, Laterra J, Hossain MA. Transgenic expression of human FGF-1 protects against hypoxic-ischemic injury in perinatal brain by intervening at caspase-XIAP signaling cascades. Neurobiol Dis 2006, 22:677-690. 10.1016/j.nbd.2006.01.016, 16635575.
66. Fujimoto M, Takagi Y, Aoki T, Hayase M, Marumo T, Gomi M, Nishimura M, Kataoka H, Hashimoto N, Nozaki K. Tissue inhibitor of metalloproteinases protect blood-brain barrier disruption in focal cerebral ischemia. J Cereb Blood Flow Metab 2008, 28:1674-1685. 10.1038/jcbfm.2008.59, 18560439.
67. Endres M, Fink K, Zhu J, Stagliano NE, Bondada V, Geddes JW, Azuma T, Mattson MP, Kwiatkowski DJ, Moskowitz MA. Neuroprotective effects of gelsolin during murine stroke. J Clin Invest 1999, 103:347-354. 10.1172/JCI4953, 407902, 9927495.