Intra-arterial bone marrow mononuclear cell transplantation correlates with GM-CSF, PDGF-BB, and MMP-2 Serum levels in stroke patients: Results from a clinical trial

Cell Transplantation

Volumn 23, Issue , 2014, Pages S57-S64

  Moniche, Francisco ^a   Montaner, Joan ^a,b   Gonzalez Marcos, Jose Ramon ^a   Carmona, Magdalena ^a   Piñero, Pilar ^a   Espigado, Ildefonso ^a   Cayuela, Aurelio ^a   Escudero, Irene ^a   de la Torre Laviana, Francisco Javier ^a   Boada, Cristina ^b   Rosell, Anna ^b   Mayol, Antonio ^a   Jimenez, Maria Dolores ^a   Gil Peralta, Alberto ^a   Gonzalez, Alejandro ^a  

^a HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^b HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

Author keywords

Cell transplantation; Growth factors (GFs); Stem cells; Stroke

Indexed keywords

GELATINASE A; GELATINASE B; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; PLATELET DERIVED GROWTH FACTOR BB;

AGED; ARTICLE; BARTHEL INDEX; BONE MARROW DERIVED MONONUCLEAR CELL; BRAIN ISCHEMIA; CELL THERAPY; CLINICAL ARTICLE; CLINICAL OUTCOME; CONTROLLED STUDY; FEMALE; FOLLOW UP; FUNCTIONAL STATUS; HUMAN; HUMAN CELL; MALE; MIDDLE CEREBRAL ARTERY; PHASE 1 CLINICAL TRIAL; PHASE 2 CLINICAL TRIAL; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL; RANKIN SCALE; SINGLE BLIND PROCEDURE; STROKE PATIENT;

EID: 85006665959     PISSN: 09636897     EISSN: 15553892     Source Type: Journal    
DOI: 10.3727/096368914X684934     Document Type: Article

References (33)

1. Barbosa da Fonseca, L. M.; Gutfilen, B.; Rosado de Castro, P. H.; Battistella, V.; Goldenberg, R. C.; Kasai-Brunswick, T.; Chagas, C. L.; Wajnberg, E.; Maiolino, A.; Salles Xavier, S.; Andre, C.; Mendez-Otero, R.; de Freitas, G. R. Migration and homing of bone-marrow mononuclear cells in chronic ischemic stroke after intra-arterial injection. Exp. Neurol. 221: 122-128 2010.
2. Brenneman, M.; Sharma, S.; Harting, M.; Strong, R.; Cox, Jr., C. S.; Aronowski, J.; Grotta, J. C.; Savitz, S. I. Autologous bone marrow mononuclear cells enhance recovery after acute ischemic stroke in young and middle aged rats. J. Cereb. Blood Flow Metab. 30: 140-149 2010.
3. Brott, T.; Adams, Jr., H. P.; Olinger, C. P.; Marler, J. R.; Barsan, W. G.; Biller, J.; Spilker, J.; Holleran, R.; Eberle, R.; Hertzberg, V. Measurements of acute cerebral infarction: A clinical examination scale. Stroke. 20: 864-870 1989.
4. Chang, D. J.; Lee, N.; Choi, C.; Jeon, I.; Oh, S. H.; Shin, D. A.; Hwang, T. S.; Lee, H. J.; Kim, S. U.; Moon, H.; Hong, K. S.; Kang, K. S.; Song, J. Therapeutic effect of BDNF overexpressing human neural stem cells (HB1.F3.BDNF) in a rodent model of middle cerebral artery occlusion. Cell Transplant. 22: 1441-1452 2013.
5. D’Olhaberriague, L.; Litvan, I.; Mitsias, P.; Mansbach, H. H. A reappraisal of reliability and validity studies in stroke. Stroke 27: 2331-2336 1996.
6. Ding, J.; Cheng, Y.; Gao, S.; Chen, J. Effects of nerve growth factor and Noggin-modified bone marrow stromal cells on stroke in rats. J. Neurosci. Res. 89: 222-230 2011.
7. Ergul, A.; Alhusban, A.; Fagan, S. C. Angiogenesis: A harmonized target for recovery after stroke. Stroke 43: 2270-2274; 2012.
8. European Stroke Organisation (ESO) Executive Committee; ESO Writing Committee. Guidelines for management of ischaemic stroke and transient ischaemic attack 2008. Cerebrovasc. Dis. 25: 457-507 2008.
9. Forsberg-Nilsson, K.; Behar, T. N.; Afrakhte, M.; Barker, J. L.; McKay, R. D. Platelet-derived growth factor induces chemotaxis of neuroepithelial stem cells. J. Neurosci. Res. 53: 521-530 1998.
10. Friedrich, M. A.; Martins, M. P.; Araújo, M. D.; Klamt, C.; Vedolin, L.; Garicochea, B.; Raupp, E. F.; Sartori El Ammar, J.; Machado, D. C.; Costa, J. C.; Nogueira, R. G.; Rosado-de-Castro, P. H.; Mendez-Otero, R.; Freitas, G. R. Intra-arterial infusion of autologous bone marrow mononuclear cells in patients with moderate to severe middle cerebral artery acute ischemic stroke. Cell Transplant. 21(Suppl 1): S13-S21; 2012.
11. Fujita, Y.; Ihara, M.; Ushiki, T.; Hirai, H.; Kizaka-Kondoh, S.; Hiraoka, M.; Ito, H.; Takahashi, R. Early protective effect of bone marrow mononuclear cells against ischemic white matter damage through augmentation of cerebral blood flow. Stroke 41: 2938-2943 2010.
12. Goldmacher, G. V.; Nasser, R.; Lee, D. Y.; Yigit, S.; Rosenwasser, R.; Iacovitti, L. Tracking transplanted bone marrow stem cells and their effects in the rat MCAO stroke model. PLoS One 8: e60049; 2013.
13. Iihoshi, S.; Honmou, O.; Houkin, K.; Hashi, K.; Kocsis, J. D. A therapeutic window for intravenous administration of autologous bone marrow after cerebral ischemia in adult rats. Brain Res. 1007: 1-9 2004.
14. Jiang, Y.; Zhu, W.; Zhu, J.; Wu, L.; Xu, G.; Liu, X. Feasibility of delivering mesenchymal stem cells via catheter to the proximal end of lesion artery in patients with stroke in the territory of middle cerebral artery. Cell Transplant. 22: 2291-2298 2013.
15. Kinnaird, T.; Stabile, E.; Burnett, M. S.; Epstein, S. E. Bone-marrow-derived cells for enhancing collateral development: Mechanisms, animal data, and initial clinical experiences. Circ. Res. 95: 354-363 2004.
16. Krupinski, J.; Issa, R.; Bujny, T.; Slevin, M.; Kumar, P.; Kumar, S.; Kaluza, J. A putative role for platelet-derived growth factor in angiogenesis and neuroprotection after ischemic stroke in humans. Stroke 28: 564-573 1997.
17. Li, Y.; Chen, J.; Zhang, C. L.; Wang, L.; Lu, D.; Katakowski, M.; Gao, Q.; Shen, L. H.; Zhang, J.; Lu, M.; Chopp, M. Gliosis and brain remodeling after treatment of stroke in rats with marrow stromal cells. Glia 49: 407-417 2005.
18. Moniche, F.; Gonzalez, A.; Gonzalez-Marcos, J. R.; Carmona, M.; Piñero, P.; Espigado, I.; Garcia-Solis, D.; Cayuela, A.; Montaner, J.; Boada, C.; Rosell, A.; Jimenez, M. D.; Mayol, A.; Gil-Peralta, A. Intra-arterial bone marrow mononuclear cells in ischemic stroke: A pilot clinical trial. Stroke 43: 2242-2244 2012.
19. Morancho, A.; Rosell, A.; García-Bonilla, L.; Montaner, J. Metalloproteinase and stroke infarct size: Role for antiinflammatory treatment? Ann. N. Y. Acad. Sci. 1207: 123-133 2010.
20. Navarro-Sobrino, M.; Rosell, A.; Hernández-Guillamon, M.; Penalba, A.; Boada, C.; Domingues-Montanari, S.; Ribó, M.; Alvarez-Sabín, J.; Montaner, J. A large screening of angiogenesis biomarkers and their association with neurological outcome after ischemic stroke. Atherosclerosis 216: 205-211 2011.
21. Ringelstein, E. B.; Thijs, V.; Norrving, B.; Chamorro, A.; Aichner, F.; Grond, M.; Saver, J.; Laage, R.; Schneider, A.; Rathgeb, F.; Vogt, G.; Charissé, G.; Fiebach, J. B.; Schwab, S.; Schäbitz, W. R.; Kollmar, R.; Fisher, M.; Brozman, M.; Skoloudik, D.; Gruber, F.; Leal, J. S.; Veltkamp, R.; Köhrmann, M.; Berrouschot, J.; for the AXIS 2 Investigators. Granulocyte colony-stimulating factor in patients with acute ischemic stroke: Results of the AX200 for ischemic stroke trial. Stroke 44: 2681-2687 2013.
22. 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.; American Heart Association Statistics Committee and Stroke Statistics Subcommittee; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics-2011 update: A report from the American Heart Association. Circulation 123: e18-e209; 2011.
23. Saito, A.; Narasimhan, P.; Hayashi, T.; Okuno, S.; Ferrand-Drake, M.; Chan, P. H. Neuroprotective role of a prolinerich Akt substrate in apoptotic neuronal cell death after stroke: Relationships with nerve growth factor. J. Neurosci. 24: 1584-1593 2004.
24. Savitz, S. I.; Misra, V.; Kasam, M.; Juneja, H.; Cox, Jr., C. S.; Alderman, S.; Aisiku, I.; Kar, S.; Gee, A.; Grotta, J. C. Intravenous autologous bone marrow mononuclear cells for ischemic stroke. Ann. Neurol. 70: 59-69 2011.
25. Schwarting, S.; Litwak, S.; Hao, W.; Bähr, M.; Weise, J.; Neumann, H. Hematopoietic stem cells reduce postischemic inflammation and ameliorate ischemic brain injury. Stroke 39: 2867-2875 2008.
26. Song, M.; Mohamad, O.; Gu, X.; Wei, L.; Yu, S. P. Restoration of intracortical and thalamocortical circuits after transplantation of bone marrow mesenchymal stem cells into the ischemic brain of mice. Cell Transplant. 22: 2001-2015 2013.
27. Sprigg, N.; Bath, P. M.; Zhao, L.; Willmot, M. R.; Gray, L. J.; Walker, M. F.; Dennis, M. S.; Russell, N. Granulocytecolony- stimulating factor mobilizes bone marrow stem cells in patients with subacute ischemic stroke: The Stem cell Trial of recovery EnhanceMent after Stroke (STEMS) pilot randomized, controlled trial (ISRCTN 16784092). Stroke 37: 2979-2983 2006.
28. Sugiyama, Y.; Yagita, Y.; Oyama, N.; Terasaki, Y.; Omura-Matsuoka, E.; Sasaki, T.; Kitagawa, K. Granulocyte colonystimulating factor enhances arteriogenesis and ameliorates cerebral damage in a mouse model of ischemic stroke. Stroke 42: 770-775 2011.
29. Takahashi, M.; Li, T. S.; Suzuki, R.; Kobayashi, T.; Ito, H.; Ikeda, Y.; Matsuzaki, M.; Hamano, K. Cytokines produced by bone marrow cells can contribute to functional improvement of the infarcted heart by protecting cardiomyocytes from ischemic injury. Am. J. Physiol. Heart Circ. Physiol. 291: H886-H893; 2006.
30. Thored, P.; Wood, J.; Arvidsson, A.; Cammenga, J.; Kokaia, Z.; Lindvall, O. Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularization after stroke. Stroke 38: 3032-3039 2007.
31. van Swieten, J. C.; Koudstaal, P. J.; Visser, M. C.; Schouten, H. J. A.; van Gijn, J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke 19: 604-607 1988.
32. Yang, Y.; Thompson, J. F.; Taheri, S.; Salayandia, V. M.; McAvoy, T. A.; Hill, J. W.; Yang, Y.; Estrada, E. Y.; Rosenberg, G. A. Early inhibition of MMP activity in ischemic rat brain promotes expression of tight junction proteins and angiogenesis during recovery. J. Cereb. Blood Flow Metab. 33: 1104-1114 2013.
33. Zhang, Z. G.; Chopp, M. Neurorestorative therapies for stroke: Underlying mechanisms and translation to the clinic. Lancet Neurol. 8: 491-500 2009.