Clinical potential of intravenous neural stem cell delivery for treatment of neuroinflammatory disease in mice?

Cell Transplantation

Volumn 20, Issue 6, 2011, Pages 851-869

  Reekmans, Kristien P ^a,b   Praet, Jelle ^a   de Vocht, Nathalie ^a   Tambuyzer, Bart R ^a   Bergwerf, Irene ^a   Daans, Jasmijn ^a   Baekelandt, Veerle ^c,d   Vanhoutte, Greetje ^a   Goossens, Herman ^a   Jorens, Philippe G ^a,b   Ysebaert, Dirk K ^a,b   Chatterjee, Shyama ^a   Pauwels, Patrick ^a   van Marck, Eric ^a   Berneman, Zwi N ^a,b   van der Linden, Annemie ^a   Ponsaerts, Peter ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b ANTWERP UNIVERSITY HOSPITAL   (Belgium)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d KU Leuven   (Belgium)

Author keywords

Bioluminescence imaging; Cell migration; Experimental autoimmune encephalomyelitis; Neural stem cells (NSCs); Transplantation

Indexed keywords

CELL MARKER; CYCLOSPORIN A; GREEN FLUORESCENT PROTEIN; IRON OXIDE; LUCIFERASE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BIOLUMINESCENCE; CELL LABELING; CELL STRUCTURE; CELL SURVIVAL; EMBRYO; FEMALE; GRAFT REJECTION; HISTOPATHOLOGY; HUMAN; LUNG CAPILLARY; MALE; MOUSE; NERVE CELL CULTURE; NEURAL STEM CELL TRANSPLANTATION; NEWBORN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PNEUMONIA; PRIORITY JOURNAL; REPORTER GENE;

ANIMALS; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; IMMUNOSUPPRESSIVE AGENTS; INJECTIONS, INTRAVENOUS; LUCIFERASES; LUMINESCENT MEASUREMENTS; MICE; MICE, TRANSGENIC; NEURAL STEM CELLS; TRANSPLANTATION, HOMOLOGOUS;

ANIMALIA; MUS;

EID: 80051749744     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368910X543411     Document Type: Article

References (57)

1. Alvarez-Buylla A.; Garcia-Verdugo J. M.; Tramontin A. D. A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2:287-293; 2001.
2. Bacigaluppi M.; Pluchino S.; Peruzotti Jametti L.; Kilic E.; Kilic U.; Salani G.; Brambilla E.; West M. J.; Comi G.; Martino G.; Hermann D. M. Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain 132:2239-2251; 2009.
3. Baekelandt V.; Eggermont K.; Michiels M.; Nuttin B.; Debyser Z. Optimized lentiviral vector production and purification procedure prevents immune response after transduction of mouse brain. Gene Ther. 10:1933-1940; 2003.
4. Baxter A. G. The origin and application of experimental autoimmune encephalomyelitis. Nat. Rev. Immunol. 7(11): 904-912; 2007.
5. Behrstock S.; Ebert A. D.; Klein S.; Schmitt M.; Moore J. M.; Svendsen C. N. Lesion-induced increase in survival and migration of human neural progenitor cells releasing GDNF. Cell Transplant. 17(7):735-762; 2008.
6. Ben-Hur T. Immunomodulation by neural stem cells. J. Neurol. Sci. 265(1-2):102-104; 2008.
7. Ben-Hur T.; Einstein O.; Mizrachi-Kol R.; Ben-Menachmen O.; Reinhartz E.; Karussis D.; Abramsky O. Transplanted multipotential neural precursor cells migrate into the inflamed white matter in response to experimental autoimmune encephalomyelitis. Glia 41:73-80; 2003.
8. Bergwerf I.; De Vocht N.; Tambuyzer B.; Verschueren J.; Reekmans K.; Daans J.; Ibrahimi A.; Van Tendeloo V.; Chatterjee S.; Goossens H.; Jorens P.; Baekelandt V.; Ysebaert D.; Van Marck E.; Berneman Z.; Van der Linden A.; Ponsaerts P. Reporter gene-expressing bone marrow-derived stromal cells are immune-tolerated following implantation in the central nervous system of syngeneic immunocompetent mice. BMC Biotechnol. 9:1; 2009.
9. Bradbury M. S.; Panagiotakos G.; Chan B. K.; Tomishima M.; Zanzonico P.; Vider J.; Ponomarev V.; Studer L.; Tabar V. Optical bioluminescence imaging of human ES cell progeny in the rodent CNS. J. Neurochem. 102(6):2029-2039; 2007.
10. Bruck W. The pathology of multiple sclerosis is the result of focal inflammatory demyelination with axonal damage. J. Neurol. 252(Suppl. 5):v3-v9; 2005.
11. Chen K.; Hughes S. M.; Conner B. Neural progenitor cells derived from the adult rat subventricular zone: Characterization and transplantation. Cell Transplant. 16(8):799-810; 2007.
12. Conti L.; Pollard S. M.; Gorba T.; Reitano E.; Toselli M.; Biella G.; Sun Y.; Sanzone S.; Ying Q. L.; Cattaneo E.; Smith A. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 9:e283; 2005.
13. Davis A. A.; Temple S. A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature 372:263-266; 1994.
14. Doetsch F. The glial identity of neural stem cells. Nat. Neurosci. 11:1127-1134; 2003.
15. Einstein O.; Fainstein N.; Vaknin I.; Mizrachi-Kol R.; Reihartz E.; Grigoriadis N.; Lavon I.; Baniyash M.; Lassmann H.; Ben-Hur T. Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression. Ann. Neurol. 61:209-218; 2007.
16. Einstein O.; Grigoriadis N.; Mizrachi-Kol R.; Reinhartz E.; Polyzoidou E.; Lavon I.; Milonas I.; Karussis D.; Abramsky O.; Ben-Hur T. Transplanted neural precursor cells reduce brain inflammation to attenuate chronic experimental autoimmune encephalomyelitis. Exp. Neurol. 198:275-284; 2006.
17. Fisher U. M.; Harting M. T.; Jimenez F.; Monzon-Posadas W. O.; Xue H.; Savitz S. I.; Laine G. A.; Cox, Jr. C. S. Pulmonary passage is a major obstacle for intravenous stem cell delivery: The pulmonary first-pass effect. Stem Cell Dev. 18(5):683-692; 2009.
18. Geraerts M.; Michiels M.; Baekelandt V.; Debyser Z.; Gijsbers R. Upscaling of lentiviral vector production by tangential flow filtration. J. Gene Med. 7:1299-1310; 2005.
19. Glaser T.; Pollard S. M.; Smith A.; Brüstle O. Tripotential differentiation of adherently expandable neural stem (NS) cells. PLoS One 2(3):e298; 2007.
20. Glavaski-Joksimovic A.; Virag T.; Chang Q. A.; West N. C.; Mangatu T. A.; McGrogan M. P.; Dugich-Djordjevic M.; Bohn M. C. Reversal of dopaminergic degeneration in a parkinsonian rat following micrografting of human bone marrow-derived neural progenitors. Cell Transplant. 18(7):801-814; 2009.
21. Gold R.; Linington C.; Lassman H. Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain 129:1953-1971; 2006.
22. Gritti A.; Frölichsthal-Schoeller P.; Galli R.; Parati E. A.; Cova L.; Pagano S. F.; Bjornson C. R.; Vescovi A. L. Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. J. Neurosci. 19:3287-3297; 1999.
23. Guzman R.; Bliss T.; De Los Angeles A.; Moseley M.; Palmer T.; Steinberg G. Neural progenitor cells transplanted into the uninjured brain undergo targeted migration after stroke onset. J. Neurosci. Res. 86:873-882; 2008.
24. Hsu Y. C.; Lee D. C.; Chiu I. M. Neural stem cells, neural progenitors, and neurotrophic factors. Cell Transplant. 16(2):133-150; 2007.
25. Ihrie R. A.; Alvarez-Buylla A. Cells in the astroglial lineage are neural stem cells. Cell Tissue Res. 331:179-191; 2008.
26. Imitola J.; Raddassi K.; In Park K.; Mueller F. J.; Nieto M.; Teng Y. D.; Frenkel D.; Li J.; Sidman R. L.; Walsh C. A.; Snyder E. Y.; Khoury S. J. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1α/CXC chemokine receptor 4 pathway. Proc. Natl. Acad. Sci. USA 101(52):18117-18122; 2004.
27. Kelly C. M.; Zietlow R.; Dunnett S. B.; Rosser A. E. The effects of various concentrations of FGF-2 on the proliferation and neuronal yield of murine embryonic neural precursor cells in vitro. Cell Transplant. 12(3):215-223; 2003.
28. Krystkowiak P.; Gaura V.; Labalette M.; Rialland A.; Remy P.; Peschanski M.; Bachoud-Lévi A. C. Alloimmunisation to donor antigens and immune rejection following foetal neural grafts to the brain in patients with Huntington's disease. PLoS One 2(1):e166; 2007.
29. Lee R. H.; Pulin A. A.; Seo M. J.; Kota D. J.; Ylostalo J.; Larson B. L.; Semprun-Prieto L.; Delafontaine P.; Prockop D. J. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 5(1):54-63; 2009.
30. Li S. H.; Lai T. Y.; Sun Z.; Han M.; Moriyama E.; Wilson B.; Fazel S.; Weisel R. D.; Yau T.; Wu J. C.; Li R. K. Tracking cardiac engraftment and distribution of implanted bone marrow cells: Comparing intra-aortic, intravenous, and intramyocardial delivery. J. Thorac. Cardiovasc. Surg. 137(5):1225-1233; 2009.
31. Lois C.; Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl. Acad. Sci. USA 90:2074-2077; 1993.
32. Lutz B. M.; Kukutsch N.; Ogilvie A. L. J.; Rößner S.; Koch F.; Romani N.; Schuler G. An advanced culture method for generating large quantities of highly purified cells from mouse bone marrow. J. Immunol. Methods 223(1):77-92; 1999.
33. McKay R. Stem cells in the central nervous system. Science 276:66-71; 1997.
34. Nohroudi K.; Arnold S.; Berhorn T.; Addicks K.; Hoehn M.; Himmelreich U. In vivo MRI stem cell tracking requires balancing of detection limit and cell viability. Cell Transplant. 19(4):431-441; 2010.
35. Okada S.; Ishii K.; Yamane J.; Iwanami A.; Ikegami T.; Katoh H.; Iwamoto Y.; Nakamura M.; Miyoshi H.; Okana H. J.; Contag C. H.; Toyama Y.; Okana H. In vivo imaging of engrafted neural stem cells: Its application in evaluating the optimal timing of transplantation for spinal cord injury. FASEB J. 19:1839-1841; 2005.
36. Parmar M.; Skogh C.; Bjrklund A.; Campbell K. Regional specification of neurosphere cultures derived from subregions of the embryonic telencephalon. Mol. Cell. Neurosci. 21:645-656; 2002.
37. Pluchino S.; Quattrini A.; Brambilla E.; Gritti A.; Salani G.; Dina G.; Galli R.; Del Carro U.; Amadio S.; Bergami A.; Furlan R.; Comi G.; Vescovi A. L.; Martino G. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422(6933):688-694; 2003.
38. Pluchino S.; Zanotti L.; Rossi B.; Brambilla E.; Ottoboni L.; Salani G.; Martinello M.; Cattalini A.; Bergami A.; Furlan R.; Comi G.; Constantin G.; Martino G. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 436(7048):266-271; 2005.
39. Politi L. S.; Bacigaluppi M.; Brambilla E.; Cadioli M.; Falini A.; Comi G.; Scotti G.; Martino G.; Pluchino S. Magnetic resonance-based tracking and quantification of intravenously injected neural stem cell accumulation in the brains of mice with experimental multiple sclerosis. Stem Cells 25:2583-2592; 2007.
40. Pollard S.; Conti L.; Smith A. Exploitation of adherent neural stem cells in basic and applied neurobiology. Regen. Med. 1:111-118; 2006.
41. Ponsaerts P.; Brown J. P.; Van den Plas D.; Van den Eeden L.; Van Bockstaele D. R.; Jorens P. G.; Van Tendeloo V. F.; Merregaert J.; Singh P. B.; Berneman Z. N. Messenger RNA electroporation is highly efficient in mouse embryonic stem cells: Successful FLPe-and Cre-mediated recombination. Gene Ther. 11:1606-1610; 2004.
42. Ponsaerts P.; Van Tendeloo V. F.; Jorens P. G.; Berneman Z. N.; Van Bockstaele D. R. Current challenges in human embryonic stem cell research: Directed differentiation and transplantation tolerance. J. Biol. Regul. Homeost. Agents 18:347-351; 2004.
43. Reynolds B. A.; Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710; 1992.
44. Richards L. J.; Kilpatrick T. J.; Bartlett P. F. De novo generation of neuronal cells from the adult mouse brain. Proc. Natl. Acad. Sci. USA 89:8591-8595; 1992.
45. Rietze R. L.; Valcanis H.; Brooker G. F.; Thomas T.; Voss A. K.; Bartlett P. F. Purification of a pluripotent neural stem cell from the adult mouse brain. Nature 412:736-739; 2001.
46. Ronsyn M. W.; Berneman Z. N.; Van Tendeloo V. F.; Jorens P. G.; Ponsaerts P. Can cell therapy heal a spinal cord injury? Spinal Cord 46:532-539; 2008.
47. Ronsyn M. W.; Daans J.; Spaepen G.; Chatterjee S.; Vermeulen K.; D'Haese P.; Van Tendeloo V. F.; Van Marck E.; Ysebaert D.; Berneman Z. N.; Jorens P. G.; Ponsaerts P. Plasmid-based genetic modification of human bone marrow-derived stromal cells: Analysis of cell survival and transgene expression after transplantation in rat spinal cord. BMC Biotechnol. 7:90; 2007.
48. Ryu M. Y.; Lee M. A.; Ahn Y. H.; Kim K. S.; Yoon S. H.; Snyder E. Y.; Cho K. G.; Kim S. U. Brain transplantation of neural stem cells cotransduced with tyrosine hydroxylase and GTP cyclohydrase 1 in Parkinsonian rats. Cell Transplant. 14(4):193-202; 2005.
49. Safran M.; Kim W. Y.; Kung A. L.; Horner J. W.; DePinho R. A.; Kaelin W. G. Mouse reporter strain for noninvasive bioluminescent imaging of cells that have undergone Cre-mediated recombination. Mol. Imaging 2:297-302; 2003.
50. Sospedra M.; Martin R. Immunology of multiple sclerosis. Annu. Rev. Immunol. 23:683-747; 2005.
51. Sun Y.; Pollard S.; Conti L.; Toselli M.; Biella G.; Parkin G.; Willatt L.; Falk A.; Cattaneo E.; Smith A. Long-term tripotent differentiation capacity of human neural stem (NS) cells in adherent culture. Mol. Cell. Neurosci. 38(2):245-258; 2008.
52. Tambuyzer B. R.; Bergwerf I.; De Vocht N.; Reekmans K.; Daans J.; Jorens P. G.; Goossens H.; Ysebaert D. K.; Chatterjee S.; Van Marck E.; Berneman Z. N.; Ponsaerts P. Allogeneic stromal cell implantation in brain tissue leads to robust microglial activation. Immunol. Cell Biol. 87(4):267-273; 2009.
53. Tropepe V.; Sibilia M.; Ciruna B. G.; Rossant J.; Wagner E. F.; van der Kooy D. Distinct neural stem cells proliferate in response to EGF and fibroblast growth factor in the developing mouse telencephalon. Dev. Biol. 208:166-188; 1999.
54. Van den Plas D.; Ponsaerts P.; Van Tendeloo V.; Van Bockstaele D. R.; Berneman Z. N.; Merregaert J. Efficient removal of LoxP-flanked genes by electroporation of Cre recombinase mRNA. Biochem. Biophys. Res. Commun. 305:10-15; 2003.
55. Wekerle H. Lessons from multiple sclerosis: Models, concepts, observations. Ann. Rheum. Dis. 67(Suppl. 3):III56-60; 2008.
56. Yang J.; Jiang Z.; Fitzgerald D. C.; Ma C.; Yu S.; Li H.; Zhao Z.; Li Y.; Ciric B.; Curtix M.; Rostami A.; Zhang G. X. Adult neural stem cells expressing IL-10 confer potent immunomodulation and remyelination in experimental autoimmune encephalitis. J. Clin. Invest. 119(12):3678-3691; 2009.
57. Zhu Q. F.; Ma J.; Yu L. L.; Yuan C. G. Grafted neural stem cells migrate to substantia nigra and improve behaviour in parkinsonian rats. Neurosci. Lett. 462:213-218; 2009.