Intracerebral injection of human mesenchymal stem cells impacts cerebral microvasculature after experimental stroke: MRI study

NMR in Biomedicine

Volumn 25, Issue 12, 2012, Pages 1340-1348

  Moisan, Anaïck ^a,b,c   Pannetier, Nicolas ^a,b   Grillon, Emmanuelle ^a,b   Richard, Marie Jeanne ^c,d   de Fraipont, Florence ^c,d   Rémy, Chantal ^a,b   Barbier, Emmanuel L ^a,b   Detante, Olivier ^a,b,c  

^a GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^b UNIV GRENOBLE ALPES   (France)

^c GRENOBLE UNIVERSITY HOSPITAL   (France)

^d INSERM   (France)

Author keywords

Angiogenesis; Cell therapy; Mesenchymal stem cells; Microvasculature; MRI; Stroke

Indexed keywords

ANGIOGENESIS; CELL THERAPY; MESENCHYMAL STEM CELL; MICRO-VASCULATURE; STROKE;

BLOOD VESSELS; CELL CULTURE; DIFFUSION; MAGNETIC RESONANCE IMAGING; RATS; STEM CELLS;

NEUROIMAGING;

ULTRASMALL SUPERPARAMAGNETIC IRON OXIDE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APPARENT DIFFUSION COEFFICIENT; ARTICLE; BLOOD VESSEL PARAMETERS; BRAIN BLOOD VESSEL; BRAIN BLOOD VOLUME; BRAIN ISCHEMIA; BRAIN MAPPING; CEREBROVASCULAR ACCIDENT; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DIFFUSION COEFFICIENT; EXPERIMENTAL MODEL; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MICROVASCULATURE; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; TREATMENT OUTCOME; VASODILATATION; VESSEL SIZE INDEX;

ANIMALS; BRAIN EDEMA; CEREBRUM; DIFFUSION; HUMANS; INJECTIONS, INTRAVENTRICULAR; MAGNETIC RESONANCE IMAGING; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICROVESSELS; RATS; STROKE;

RATTUS;

EID: 84868151948     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.2806     Document Type: Article

References (47)

1. Lloyd-Jones D, Adams R, Carnethon M, De Simone G, Ferguson TB, Flegal K, Ford E, Furie K, Go A, Greenlund K, Haase N, Hailpern S, Ho M, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott M, Meigs J, Mozaffarian D, Nichol G, O'Donnell C, Roger V, Rosamond W, Sacco R, Sorlie P, Stafford R, Steinberger J, Thom T, Wasserthiel-Smoller S, Wong N, Wylie-Rosett J, Hong Y. Heart disease and stroke statistics - 2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2009; 119: 480-486.
2. Burns TC, Steinberg GK. Stem cells and stroke: opportunities, challenges and strategies. Expert Opin. Biol. Ther. 2011; 11: 447-461.
3. Lindvall O, Kokaia Z. Recovery and rehabilitation in stroke: stem cells. Stroke 2004; 35: 2691-2694.
4. Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 2007; 25: 2739-2749.
5. 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.
6. Detante O, Moisan A, Dimastromatteo J, Richard MJ, Riou L, Grillon E, Barbier E, Desruet MD, De Fraipont F, Segebarth C, Jaillard A, Hommel M, Ghezzi C, Remy C. Intravenous administration of Tc-99m-HMPAO-labeled human mesenchymal stem cells after stroke: in vivo imaging and biodistribution. Cell Transplant. 2009; 18: 1369-1379.
7. Bang OY, Lee JS, Lee PH, Lee G. Autologous mesenchymal stem cell transplantation in stroke patients. Ann. Neurol. 2005; 57: 874-882.
8. Lee JS, Hong JM, Moon GJ, Lee PH, Ahn YH, Bang OY. A long-term follow-up study of intravenous autologous mesenchymal stem cell transplantation in patients with ischemic stroke. Stem Cells 2010; 28: 1099-1106.
9. Honmou O, Houkin K, Matsunaga T, Niitsu Y, Ishiai S, Onodera R, Waxman SG, Kocsis JD Intravenous administration of auto serum-expanded autologous mesenchymal stem cells in stroke. Brain 2011; 134: 1790-1807.
10. Horita Y, Honmou O, Harada K, Houkin K, Hamada H, Kocsis JD. Intravenous administration of glial cell line-derived neurotrophic factor gene-modified human mesenchymal stem cells protects against injury in a cerebral ischemia model in the adult rat. J. Neurosci. Res. 2006; 84: 1495-1504.
11. Liu H, Honmou O, Harada K, Nakamura K, Houkin K, Hamada H, Kocsis JD. Neuroprotection by PlGF gene-modified human mesenchymal stem cells after cerebral ischaemia. Brain 2006; 129: 2734-2745.
12. Omori Y, Honmou O, Harada K, Suzuki J, Houkin K, Kocsis JD. Optimization of a therapeutic protocol for intravenous injection of human mesenchymal stem cells after cerebral ischemia in adult rats. Brain Res. 2008; 1236: 30-38.
13. Onda T, Honmou O, Harada K, Houkin K, Hamada H, Kocsis JD. Therapeutic benefits by human mesenchymal stem cells (hMSCs) and Ang-1 gene-modified hMSCs after cerebral ischemia. J. Cereb. Blood Flow Metab. 2008; 28: 329-340.
14. Toyama K, Honmou O, Harada K, Suzuki J, Houkin K, Hamada H, Kocsis JD. Therapeutic benefits of angiogenetic gene-modified human mesenchymal stem cells after cerebral ischemia. Exp. Neurol. 2009; 216: 47-55.
15. Nomura T, Honmou O, Harada K, Houkin K, Hamada H, Kocsis JD. I.V. infusion of brain-derived neurotrophic factor gene-modified human mesenchymal stem cells protects against injury in a cerebral ischemia model in adult rat. Neuroscience 2005; 136: 161-169.
16. Chen J, Li Y, Zhang R, Katakowski M, Gautam SC, Xu Y, Lu M, Zhang Z, Chopp M. Combination therapy of stroke in rats with a nitric oxide donor and human bone marrow stromal cells enhances angiogenesis and neurogenesis. Brain Res. 2004; 1005: 21-28.
17. 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.
18. 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.
19. Zhang J, Li Y, Chen J, Yang M, Katakowski M, Lu M, Chopp M. Expression of insulin-like growth factor 1 and receptor in ischemic rats treated with human marrow stromal cells. Brain Res. 2004; 1030: 19-27.
20. Zhao LR, Duan WM, Reyes M, Keene CD, Verfaillie CM, Low WC. Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological deficits after grafting into the ischemic brain of rats. Exp. Neurol. 2002; 174: 11-20.
21. Dirnagl U, Iadecola C, Moskowitz MA. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 1999; 22: 391-397.
22. Plate KH. Mechanisms of angiogenesis in the brain. J. Neuropathol. Exp. Neurol. 1999; 58: 313-320.
23. Krupinski J, Kaluza J, Kumar P, Kumar S, Wang JM. Role of angiogenesis in patients with cerebral ischemic stroke. Stroke 1994; 25: 1794-1798.
24. Lin CY, Chang C, Cheung WM, Lin MH, Chen JJ, Hsu CY, Chen JH, Lin TN. Dynamic changes in vascular permeability, cerebral blood volume, vascular density, and size after transient focal cerebral ischemia in rats: evaluation with contrast-enhanced magnetic resonance imaging. J. Cereb. Blood Flow Metab. 2008; 28: 1491-1501.
25. Longa EZ, Weinstein PR, Carlson S, Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989; 20: 84-91.
26. Moriscot C, de Fraipont F, Richard MJ, Marchand M, Savatier P, Bosco D, Favrot M, Benhamou PY. Human bone marrow mesenchymal stem cells can express insulin and key transcription factors of the endocrine pancreas developmental pathway upon genetic and/or microenvironmental manipulation in vitro. Stem Cells 2005; 23: 594-603.
27. Detante O, Valable S, De Fraipont F, Grillon E, Barbier EL, Moisan A, Arnaud J, Moriscot C, Segebarth C, Hommel M, Rémy C, Richard M-J. MRI and fluorescence labeling of clinical grade mesenchymal stem cells without impacting their phenotype: study in a rat model of stroke. Stem Cells Translational Med. 2012. DOI: 10.5966/sctm.2011-0043.
28. Tropres I, Grimault S, Vaeth A, Grillon E, Julien C, Payen JF, Lamalle L, Decorps M. Vessel size imaging. Magn. Reson. Med. 2001; 45: 397-408.
29. Valable S, Lemasson B, Farion R, Beaumont M, Segebarth C, Remy C, Barbier EL. Assessment of blood volume, vessel size, and the expression of angiogenic factors in two rat glioma models: a longitudinal in vivo and ex vivo study. NMR Biomed. 2008; 21: 1043-1056.
30. Neumann-Haefelin T, Kastrup A, de Crespigny A, Yenari MA, Ringer T, Sun GH, Moseley ME. Serial MRI after transient focal cerebral ischemia in rats: dynamics of tissue injury, blood-brain barrier damage, and edema formation. Stroke 2000; 31: 1965-1972; discussion 1972-1973.
31. Beaumont M, Lemasson B, Farion R, Segebarth C, Remy C, Barbier EL. Characterization of tumor angiogenesis in rat brain using iron-based vessel size index MRI in combination with gadolinium-based dynamic contrast-enhanced MRI. J. Cereb. Blood Flow Metab. 2009; 29: 1714-1726.
32. Keunen O, Johansson M, Oudin A, Sanzey M, Rahim SA, Fack F, Thorsen F, Taxt T, Bartos M, Jirik R, Miletic H, Wang J, Stieber D, Stuhr L, Moen I, Rygh CB, Bjerkvig R, Niclou SP. Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc. Natl. Acad. Sci. USA 2011; 108: 3749-3754.
33. Tropres I, Lamalle L, Peoc'h M, Farion R, Usson Y, Decorps M, Remy C. In vivo assessment of tumoral angiogenesis. Magn. Reson. Med. 2004; 51: 533-541.
34. Lemasson B, Christen T, Tizon X, Farion R, Fondraz N, Provent P, Segebarth C, Barbier EL, Genne P, Duchamp O, Remy C. Assessment of multiparametric MRI in a human glioma model to monitor cytotoxic and anti-angiogenic drug effects. NMR Biomed. 2010; 24: 473-482.
35. Pannetier N, Lemasson B, Christen T, Tachrount M, Tropres I, Farion R, Segebarth C, Remy C, Barbier EL. Vessel size index measurements in a rat model of glioma: comparison of the dynamic (Gd) and steady-state (iron-oxide) susceptibility contrast MRI approaches. NMR Biomed. 2012; 25: 218-226.
36. Lin TN, Sun SW, Cheung WM, Li F, Chang C. Dynamic changes in cerebral blood flow and angiogenesis after transient focal cerebral ischemia in rats. Evaluation with serial magnetic resonance imaging. Stroke 2002; 33: 2985-2891.
37. Komatsu K, Honmou O, Suzuki J, Houkin K, Hamada H, Kocsis JD. Therapeutic time window of mesenchymal stem cells derived from bone marrow after cerebral ischemia. Brain Res. 2010; 1334: 84-92.
38. Kode JA, Mukherjee S, Joglekar MV, Hardikar AA. Mesenchymal stem cells: immunobiology and role in immunomodulation and tissue regeneration. Cytotherapy 2009; 11: 377-391.
39. Sanz L, Santos-Valle P, Alonso-Camino V, Salas C, Serrano A, Vicario JL, Cuesta AM, Compte M, Sanchez-Martin D, Alvarez-Vallina L. Long-term in vivo imaging of human angiogenesis: critical role of bone marrow-derived mesenchymal stem cells for the generation of durable blood vessels. Microvasc. Res. 2008; 75: 308-314.
40. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J. Cell. Biochem. 2006; 98: 1076-1084.
41. Au P, Tam J, Fukumura D, Jain RK. Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 2008; 111: 4551-4558.
42. Kojima T, Hirota Y, Ema M, Takahashi S, Miyoshi I, Okano H, Sawamoto K. Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the post-stroke striatum. Stem Cells 2010; 28: 545-554.
43. Ohab JJ, Fleming S, Blesch A, Carmichael ST. A neurovascular niche for neurogenesis after stroke. J. Neurosci. 2006; 26: 13 007-13 016.
44. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005; 105: 1815-1822.
45. Witte OW, Stoll G. Delayed and remote effects of focal cortical infarctions: secondary damage and reactive plasticity. Adv. Neurol. 1997; 73: 207-227.
46. Manoonkitiwongsa PS, Jackson-Friedman C, McMillan PJ, Schultz RL, Lyden PD. Angiogenesis after stroke is correlated with increased numbers of macrophages: the clean-up hypothesis. J. Cereb. Blood Flow Metab. 2001; 21: 1223-1231.
47. Yu SW, Friedman B, Cheng Q, Lyden PD. Stroke-evoked angiogenesis results in a transient population of microvessels. J. Cereb. Blood Flow Metab. 2007; 27: 755-763.