Intra-Arterial Transplantation of Low-Dose Stem Cells Provides Functional Recovery Without Adverse Effects After Stroke

Cellular and Molecular Neurobiology

Volumn 35, Issue 3, 2015, Pages 399-406

  Fukuda, Yuhtaka ^a   Horie, Nobutaka ^a   Satoh, Katsuya ^a   Yamaguchi, Susumu ^a   Morofuji, Youichi ^a   Hiu, Takeshi ^a   Izumo, Tsuyoshi ^a   Hayashi, Kentaro ^a   Nishida, Noriyuki ^a   Nagata, Izumi ^a  

^a NAGASAKI UNIVERSITY   (Japan)

Author keywords

Dose; Intra arterial transplantation; Mesenchymal stem cells; Stroke

Indexed keywords

INTERLEUKIN 12P70; INTERLEUKIN 1BETA;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BRAIN CORTEX; BRAIN EMBOLISM; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL COUNT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CONVALESCENCE; CORPUS STRIATUM; HISTOPATHOLOGY; HUMAN; HUMAN CELL; INFLAMMATION; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MORTALITY; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; RISK REDUCTION; ADVERSE EFFECTS; ANIMAL; CELL CULTURE; FEMALE; INTRAARTERIAL DRUG ADMINISTRATION; PATHOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT; STROKE; YOUNG ADULT;

ANIMALS; CELLS, CULTURED; FEMALE; HUMANS; INFUSIONS, INTRA-ARTERIAL; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; STROKE; YOUNG ADULT;

EID: 84925533654     PISSN: 02724340     EISSN: 15736830     Source Type: Journal    
DOI: 10.1007/s10571-014-0135-9     Document Type: Article

References (35)

1. Abe K, Yamashita T, Takizawa S, Kuroda S, Kinouchi H, Kawahara N (2012) Stem cell therapy for cerebral ischemia: from basic science to clinical applications. J Cereb Blood Flow Metab 32:1317–1331
2. Amar AP, Zlokovic BV, Apuzzo MLJ (2003) Endovascular restorative neurosurgery: a novel concept for molecular and cellular therapy of the nervous system. Neurosurgery 52:402–413
3. Andres RH, Choi R, Pendharkar AV, Gaeta X, Wang N, Nathan JK, Chua JY, Lee SW, Palmer TD, Steinberg GK, Guzman R (2011a) The CCR2/CCL2 interaction mediates the transendothelial recruitment of intravascularly delivered neural stem cells to the ischemic brain. Stroke 42:2923–2931
4. Andres RH, Horie N, Slikker W, Keren-Gill H, Zhan K, Sun G, Manley NC, Pereira MP, Sheikh LA, McMillan EL, Schaar BT, Svendsen CN, Bliss TM, Steinberg GK (2011b) Human neural stem cells enhance structural plasticity and axonal transport in the ischaemic brain. Brain 134:1777–1789
5. Bliss T, Guzman R, Daadi M, Steinberg GK (2007) Cell transplantation therapy for stroke. Stroke 38:817–826
6. Boutin H, LeFeuvre RA, Horai R, Asano M, Iwakura Y, Rothwell NJ (2001) Role of IL-1alpha and IL-1beta in ischemic brain damage. J Neurosci 21:5528–5534
7. Byun JS, Kwak BK, Kim JK, Jung J, Ha BC, Park S (2013) Engraftment of human mesenchymal stem cells in a rat photothrombotic cerebral infarction model: comparison of intra-arterial and intravenous infusion using MRI and histological analysis. J Korean Neurosurg Soc 54:467–476
8. Chen J, Li Y, Wang L, Zhang Z, Lu D, Lu M, Chopp M (2001) Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 32:1005–1011
9. Chua JY, Pendharkar AV, Wang N, Choi R, Andres RH, Gaeta X, Zhang J, Moseley ME, Guzman R (2011) Intra-arterial injection of neural stem cells using a microneedle technique does not cause microembolic strokes. J Cereb Blood Flow Metab 31:1263–1271
10. Eckert MA, Vu Q, Xie K, Yu J, Liao W, Cramer SC, Zhao W (2013) Evidence for high translational potential of mesenchymal stromal cell therapy to improve recovery from ischemic stroke. J Cereb Blood Flow Metab 33:1322–1334
11. Encarnacion A, Horie N, Keren-Gill H, Bliss TM, Steinberg GK, Shamloo M (2011) Long-term behavioral assessment of function in an experimental model for ischemic stroke. J Neurosci Methods 196:247–257
12. Gutierrez-Fernandez M, Rodriguez-Frutos B, Alvarez-Grech J, Vallejo-Cremades MT, Exposito-Alcaide M, Merino J, Roda JM, Diez-Tejedor E (2011) Functional recovery after hematic administration of allogenic mesenchymal stem cells in acute ischemic stroke in rats. Neuroscience 175:394–405
13. Guzman R, Choi R, Gera A, De Los Angeles A, Andres RH, Steinberg GK (2008a) Intravascular cell replacement therapy for stroke. Neurosurg Focus 24:E15
14. Guzman R, De Los Angeles A, Cheshier S, Choi R, Hoang S, Liauw J, Schaar B, Steinberg G (2008b) Intracarotid injection of fluorescence activated cell-sorted CD49d-positive neural stem cells improves targeted cell delivery and behavior after stroke in a mouse stroke model. Stroke 39:1300–1306
15. Horie N, Maag AL, Hamilton SA, Shichinohe H, Bliss TM, Steinberg GK (2008) Mouse model of focal cerebral ischemia using endothelin-1. J Neurosci Methods 173:286–290
16. Horie N, Pereira MP, Niizuma K, Sun G, Keren-Gill H, Encarnacion A, Shamloo M, Hamilton SA, Jiang K, Huhn S, Palmer TD, Bliss TM, Steinberg GK (2011) Transplanted stem cell-secreted vascular endothelial growth factor effects poststroke recovery, inflammation, and vascular repair. Stem Cells 29:274–285
17. Ishizaka S, Horie N, Satoh K, Fukuda Y, Nishida N, Nagata I (2013) Intra-arterial cell transplantation provides timing-dependent cell distribution and functional recovery after stroke. Stroke 44:720–726
18. Janowski M, Lyczek A, Engels C, Xu J, Lukomska B, Bulte JW, Walczak P (2013) Cell size and velocity of injection are major determinants of the safety of intracarotid stem cell transplantation. J Cereb Blood Flow Metab 33:921–927
19. Kamiya N, Ueda M, Igarashi H, Nishiyama Y, Suda S, Inaba T, Katayama Y (2008) Intra-arterial transplantation of bone marrow mononuclear cells immediately after reperfusion decreases brain injury after focal ischemia in rats. Life Sci 83:433–437
20. Li Y, Chen J, Wang L, Lu M, Chopp M (2001) Treatment of stroke in rat with intracarotid administration of marrow stromal cells. Neurology 56:1666–1672
21. Lindvall O, Kokaia Z (2011) Stem cell research in stroke: how far from the clinic? Stroke 42:2369–2375
22. Liu H, Honmou O, Harada K, Nakamura K, Houkin K, Hamada H, Kocsis JD (2006) Neuroprotection by PlGF gene-modified human mesenchymal stem cells after cerebral ischaemia. Brain 129:2734–2745
23. McGuckin CP, Jurga M, Miller AM, Sarnowska A, Wiedner M, Boyle NT, Lynch MA, Jablonska A, Drela K, Lukomska B, Domanska-Janik K, Kenner L, Moriggl R, Degoul O, Perruisseau-Carrier C, Forraz N (2013) Ischemic brain injury: a consortium analysis of key factors involved in mesenchymal stem cell-mediated inflammatory reduction. Arch Biochem Biophys 534:88–97
24. Messina LM, Podrazik RM, Whitehill TA, Ekhterae D, Brothers TE, Wilson JM, Burkel WE, Stanley JC (1992) Adhesion and incorporation of lacZ-transduced endothelial cells into the intact capillary wall in the rat. Proc Natl Acad Sci USA 89:12018–12022
25. Misra V, Ritchie MM, Stone LL, Low WC, Janardhan V (2012) Stem cell therapy in ischemic stroke: role of IV and intra-arterial therapy. Neurology 79:S207–S212
26. Mitkari B, Nitzsche F, Kerkela E, Kuptsova K, Huttunen J, Nystedt J, Korhonen M, Jolkkonen J (2014) Human bone marrow mesenchymal stem/stromal cells produce efficient localization in the brain and enhanced angiogenesis after intra-arterial delivery in rats with cerebral ischemia, but this is not translated to behavioral recovery. Behav Brain Res 259:50–59
27. Murphy TH, Corbett D (2009) Plasticity during stroke recovery: from synapse to behaviour. Nat Rev Neurosci 10:861–872
28. Pendharkar AV, Chua JY, Andres RH, Wang N, Gaeta X, Wang H, De A, Choi R, Chen S, Rutt BK, Gambhir SS, Guzman R (2010) Biodistribution of neural stem cells after intravascular therapy for hypoxic-ischemia. Stroke 41:2064–2070
29. Rosado-de-Castro PH, Pimentel-Coelho PM, da Fonseca LM, de Freitas GR, Mendez-Otero R (2013) The rise of cell therapy trials for stroke: review of published and registered studies. Stem Cells Dev 22:2095–2111
30. Rosenblum S, Wang N, Smith TN, Pendharkar AV, Chua JY, Birk H, Guzman R (2012) Timing of intra-arterial neural stem cell transplantation after hypoxia-ischemia influences cell engraftment, survival, and differentiation. Stroke 43:1624–1631
31. Shichita T, Ago T, Kamouchi M, Kitazono T, Yoshimura A, Ooboshi H (2012) Novel therapeutic strategies targeting innate immune responses and early inflammation after stroke. J Neurochem 123(Suppl 2):29–38
32. Stem Cell Therapies as an Emerging Paradigm in Stroke (STEPS) (2009) Bridging basic and clinical science for cellular and neurogenic factor therapy in treating stroke. Stroke 40:510–515
33. Walczak P, Zhang J, Gilad AA, Kedziorek DA, Ruiz-Cabello J, Young RG, Pittenger MF, van Zijl PC, Huang J, Bulte JW (2008) Dual-modality monitoring of targeted intraarterial delivery of mesenchymal stem cells after transient ischemia. Stroke 39:1569–1574
34. Yang B, Migliati E, Parsha K, Schaar K, Xi X, Aronowski J, Savitz SI (2013) Intra-arterial delivery is not superior to intravenous delivery of autologous bone marrow mononuclear cells in acute ischemic stroke. Stroke 44:3463–3472
35. Yavagal DR, Lin B, Raval AP, Garza PS, Dong C, Zhao W, Rangel EB, McNiece I, Rundek T, Sacco RL, Perez-Pinzon M, Hare JM (2014) Efficacy and dose-dependent safety of intra-arterial delivery of mesenchymal stem cells in a rodent stroke model. PLoS ONE 9:e93735