Different methods of immunosuppresion do not prolong the survival of human cord blood-derived neural stem cells transplanted into focal brain-injured immunocompetent rats

Acta Neurobiologiae Experimentalis

Volumn 73, Issue 1, 2013, Pages 88-101

  Jablonska, Anna ^a   Janowski, Mirosław ^a,b   Lukomska, Barbara ^a  

^a MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell transplantation; Cord blood cells; Desensitization; Focal brain injury; Immunosuppression; Neural progenitors

Indexed keywords

EID: 84878383424     PISSN: 00651400     EISSN: 16890035     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Ali H, Forraz N, McGuckin CP, Jurga M, Lindsay S, Ip BK, Trevelyan A, Basford C, Habibollah S, Ahmad S, Clowry GJ, Bayatti N (2012) In vitro modelling of cortical neurogenesis by sequential induction of human umbilical cord blood stem cells. Stem Cell Rev 8: 210-223.
2. Anderson MF, Blomstrand F, Blomstrand C, Eriksson PS, Nilsson M (2003) Astrocytes and stroke: networking for survival? Neurochem Res 28: 293-305.
3. Armstrong RJ, Harrower TP, Hurelbrink CB, McLaughin M, Ratcliffe EL, Tyers P, Richards A, Dunnett SB, Rosser AE, Barker RA (2001) Porcine neural xenografts in the immunocompetent rat: immune response following grafting of expanded neural precursor cells. Neuroscience 106: 201-216.
4. Bergwerf I, De Vocht N, Tambuyzer B, Verschueren J, Reekmans K, Daans J, Ibrahimi A, Van Tendeloo V, Chatterjee S, Goossens H, Jorens PG, Baekelandt V, Ysebaert D, Van Marck E, Berneman ZN, Linden AV, Ponsaerts P (2009) Reporter gene-expressing bone marrow-derived stromal cells are immune-tolerated following implantation in the central nervous system of syngeneic immunocompetent mice. BMC Biotechnol 7: 9-11.
5. Borlongan CV, Hadman M, Sanberg CD, Sanberg PR (2004) Central nervous system entry of peripherally injected umbilical cord blood cells is not required for neuroprotection in stroke. Stroke 35: 2385-2389.
6. Buzanska L, Machaj EK, Zablocka B, Pojda Z, Domanska-Janik K (2002) Human cord blood-derived cells attain neuronal and glial features in vitro. J Cell Sci 115: 2131-2138.
7. Buzanska L, Jurga M, Stachowiak EK, Stachowiak MK, Domańska-Janik K (2006) Neural stem-like cell line derived from a nonhematopoietic population of human umbilical cord blood. Stem Cells Dev 15: 391-406.
8. Chen J, Sanberg PR, Li Y, Wang L, Lu M, Willing AE, Sanchez-Ramos J, Chopp M (2001) Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats. Stroke 32: 2682-2688.
9. Chen Z, Palmer TD (2008) Cellular repair of CNS disorders: an immunological perspective. Hum Mol Genet 17(R1): R84-92.
10. Coyne TM, Marcus AJ, Woodbury D, Black IB (2006) Marrow stromal cells transplanted to the adult brain are rejected by an inflammatory response and transfer donor labels to host neurons and glia. Stem Cells 24: 2483-2492.
11. Dubois-Dauphin M, Julien S (2010) Stem cell-derived neurons grafted in the striatum are expelled out of the brain after chronic cortical stroke. Stroke 41: 1807-1814.
12. Glover JC, Boulland JL, Halasi G, Kasumacic N (2010) Chimeric animal models in human stem cell biology. ILAR Journal 51: 62-73.
13. Gorelik M, Janowski M, Galpoththawela C, Rifkin R, Levy M, Lukomska B, Kerr DA, Bulte JW, Walczak P (2012) Non-invasive monitoring of immunosuppressive drug efficacy to prevent rejection of intracerebral glial precursor allografts. Cell Transplant 21: 2149-2157.
14. Gornicka-Pawlak E, Janowski M, Habich A, Jablonska A, Drela K, Kozlowska H, Lukomska B, Domanska-Janik K (2011) Systemic treatment of focal brain injury in the rat by human umbilical cord blood cells being at different level of neural commitment. Acta Neurobiol Exp (Wars) 71: 46-64.
15. Haas S, Weidner N, Winkler J (2005) Adult stem cell therapy in stroke. Curr Opin Neurol 18: 59-64.
16. Habich A, Jurga M, Markiewicz I, Lukomska B, Bany-Laszewicz U, Domanska-Janik K (2006) Early appearance of stem/progenitor cells with neural-like characteristics in human cord blood mononuclear fraction cultured in vitro. Exp Hematol 34: 914-925.
17. Hermann A, Gastl R, Liebau S, Popa MO, Fiedler J, Boehm BO, Maisel M, Lerche H, Schwarz J, Brenner R, Storch A (2004) Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J Cell Sci 117: 4411-4422.
18. Hicks AU, Lappalainen RS, Narkilahti S, Suuronen R, Corbett D, Sivenius J, Hovatta O, Jolkkonen J (2009) Transplantation of human embryonic stem cell-derived neural precursor cells and enriched environment after cortical stroke in rats: cell survival and functional recovery. Eur J Neurosci 29: 562-574.
19. Hofmeijer J, Veldhuis WB, Schepers J, Nicolay K, Kappelle LJ, Bär PR, van der Worp HB (2004) The time course of ischemic damage and cerebral perfusion in a rat model of space-occupying cerebral infarction. Brain Res 1013: 74-82.
20. Hovakimyan M, Müller J, Wree A, Ortinau S, Rolfs A, Schmitt O (2012) Survival of transplanted human neural stem cell line (ReNcell VM) into the rat brain with and without immunosuppression. Ann Anat 194: 429-435.
21. Jablonska A, Kozlowska H, Markiewicz I, Domanska-Janik K, Lukomska B (2010) Transplantation of neural stem cells derived from human cord blood to the brain of adult and neonatal rats. Acta Neurobiol Exp (Wars) 70: 337-350.
22. Janowski M, Gornicka-Pawlak E, Kozlowska H, Domanska-Janik K, Gielecki J, Lukomska B (2008) Structural and functional characteristic of a model for deep-seated lacunar infarct in rats. J Neurol Sci 273: 40-48.
23. Janowski M, Jablonska A, Kozlowska H, Orukari I, Bernard S, Bulte JW, Lukomska B, Walczak P (2012) Neonatal desensitization does not universally prevent xenograft rejection. Nat Methods 9: 856-858.
24. Jin K, Wang X, Xie L, Mao XO, Zhu W, Wang Y, Shen J, Mao Y, Banwait S, Greenberg DA (2006) Evidence for stroke-induced neurogenesis in the human brain. Proc Natl Acad Sci U S A 103: 13198-13202.
25. Jurga M, Markiewicz I, Sarnowska A, Habich A, Kozłowska H, Lukomska B, Buzańska L, Domańska-Janik K (2006) Neurogenic potential of human umbilical cord blood: neural-like stem cells depend on previous long-term culture conditions. J Neurosci Res 83: 627-637.
26. Jurga M, Lipkowski AW, Lukomska B, Buzanska L, Kurzepa K, Sobanski T, Habich A, Coecke S, Gajkowska B, Domanska-Janik K (2009) Generation of functional neural artificial tissue from human umbilical cord blood stem cells. Tissue Eng Part C Methods 15: 365-372.
27. Jurga M, Dainiak MB, Sarnowska A, Jablonska A, Tripathi A, Plieva FM, Savina IN, Strojek L, Jungvid H, Kumar A, Lukomska B, Domanska-Janik K, Forraz N, McGuckin CP (2011) The performance of laminin-containing cryogel scaffolds in neural tissue regeneration. Biomaterials 32: 3423-3434.
28. Kelly CM, Precious SV, Scherf C, Penketh R, Amso NN, Battersby A, Allen ND, Dunnett SB, Rosser AE (2009) Neonatal desensitization allows long-term survival of neural xenotransplants without immunosuppression. Nat Methods 6: 271-273.
29. Kelly S, Bliss TM, Shah AK, Sun GH, Ma M, Foo WC, Masel J, Yenari MA, Weissman IL, Uchida N, Palmer T, Steinberg GK (2004) Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc Natl Acad Sci U S A 101: 11839-11844.
30. Kögler G, Sensken S, Airey JA, Trapp T, Müschen M, Feldhahn N, Liedtke S, Sorg RV, Fischer J, Rosenbaum C, Greschat S, Knipper A, Bender J, Degistirici O, Gao J, Caplan AI, Colletti EJ, Almeida-Porada G, Müller HW, Zanjani E, Wernet P (2004) A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J Exp Med 200: 123-135.
31. Kozłowska H, Jabłonka J, Janowski M, Jurga M, Kossut M, Domańska-Janik K (2007) Transplantation of a novel human cord blood-derived neural-like stem cell line in a rat model of cortical infarct. Stem Cells Dev 16: 481-488.
32. Kuh SU, Cho YE, Yoon DH, Kim KN, Ha Y (2005) Functional recovery after human umbilical cord blood cells transplantation with brain-derived neutrophic factor into the spinal cord injured rat. Acta Neurochir (Wien) 147: 985-992.
33. Larsson LC, Widner H (2000) Neural tissue xenografting. Scand J Immunol 52: 249-256.
34. Larsson LC, Frielingsdorf H, Mirza B, Hansson SJ, Anderson P, Czech KA, Strandberg M, Widner H (2001) Porcine neural xenografts in rats and mice: donor tissue development and characteristics of rejection. Exp Neurol 172: 100-114.
35. Lindvall O, Kokaia Z (2005) Stem cell therapy for human brain disorders. Kidney Int 68: 1937-1939.
36. Liu HY, Zhang QJ, Li HJ, Han ZC (2006) Effect of intracranial transplantation of CD34+ cells derived from human umbilical cord blood in rats with cerebral ischemia. Chin Med J (Engl) 119: 1744-1748.
37. McGuckin CP, Forraz N, Allouard Q, Pettengell R (2004) Umbilical cord blood stem cells can expand hematopoietic and neuroglial progenitors in vitro. Exp Cell Res 295: 350-359.
38. Meier C, Middelanis J, Wasielewski B, Neuhoff S, Roth-Haerer A, Gantert M, Dinse HR, Dermietzel R, Jensen A (2006) Spastic paresis after perinatal brain damage in rats is reduced by human cord blood mononuclear cells. Pediatr Res 59: 244-249.
39. Molcanyi M, Riess P, Bentz K, Maegele M, Hescheler J, Schäfke B, Trapp T, Neugebauer E, Klug N, Schäfer U (2007) Trauma-associated inflammatory response impairs embryonic stem cell survival and integration after implantation into injured rat brain. J Neurotrauma 24: 625-637.
40. Munoz JR, Stoutenger BR, Robinson AP, Spees JL, Prockop DJ (2005) Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc Natl Acad Sci U S A 102: 18171-18176.
41. Neuhoff S, Moers J, Rieks M, Grunwald T, Jensen A, Dermietzel R, Meier C (2007) Proliferation, differentiation, and cytokine secretion of human umbilical cord blood-derived mononuclear cells in vitro. Exp Hematol 35: 1119-1131.
42. Niranjan A, Fellows W, Stauffer W, Burton EA, Hong CS, Lunsford LD, Kondziolka D, Glorioso JC, Gobbel GT (2007) Survival of transplanted neural progenitor cells enhanced by brain irradiation. J Neurosurg 107: 383-391.
43. Olstorn H, Moe MC, Røste GK, Bueters T, Langmoen IA (2007) Transplantation of stem cells from the adult human brain to the adult rat brain. Neurosurgery 60: 1089-1098.
44. Pan Y, Nastav JB, Zhang H, Bretton RH, Panneton WM, Bicknese AR (2005) Engraftment of freshly isolated or cultured human umbilical cord blood cells and the effect of cyclosporin A on the outcome. Exp Neurol 192: 365-372.
45. Pedersen EB, Zimmer J, Finsen B (1997) Triple immunosuppression protects murine intracerebral, hippocampal xenografts in adult rat hosts: effects on cellular infiltration, major histocompatibility complex antigen induction and blood-brain barrier leakage. Neuroscience 78: 685-701.
46. Pluchino S, Zanotti L, Deleidi M, Martino G (2005) Neural stem cells and their use as therapeutic tool in neurological disorders. Brain Res Brain Res Rev 48: 211-219.
47. Rosen CL, Dinapoli VA, Nagamine T, Crocco T (2005) Influence of age on stroke outcome following transient focal ischemia. J Neurosurg 103: 687-694.
48. Rota Nodari L, Ferrari D, Giani F, Bossi M, Rodriguez-Menendez V, Tredici G, Delia D, Vescovi AL, De Filippis L (2010) Long-term survival of human neural stem cells in the ischemic rat brain upon transient immunosuppression. PLoS One 5: e14035.
49. Ruiz A, Buzanska L, Gilliland D, Rauscher H, Sirghi L, Sobanski T, Zychowicz M, Ceriotti L, Bretagnol F, Coecke S, Colpo P, Rossi F (2008) Micro-stamped surfaces for the patterned growth of neural stem cells. Biomaterials 29: 4766-4774.
50. Sanchez-Ramos JR, Song S, Kamath SG, Zigova T, Willing A, Cardozo-Pelaez F, Stedeford T, Chopp M, Sanberg PR (2001) Expression of neural markers in human umbilical cord blood. Exp Neurol 171: 109-115.
51. Steiner B, Roch M, Holtkamp N, Kurtz A (2012) Systemically administered human bone marrow-derived mesenchymal stem home into peripheral organs but do not induce neuroprotective effects in the MCAo-mouse model for cerebral ischemia. Neurosci Lett 513: 25-30.
52. Sun W, Buzanska L, Domanska-Janik K, Salvi RJ, Stachowiak MK (2005) Voltage-sensitive and ligandgated channels in differentiating neural stem-like cells derived from the nonhematopoietic fraction of human umbilical cord blood. Stem Cells 23: 931-945.
53. Taguchi A, Soma T, Tanaka H, Kanda T, Nishimura H, Yoshikawa H, Tsukamoto Y, Iso H, Fujimori Y, Stern DM, Naritomi H, Matsuyama T (2004) Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J Clin Invest 114: 330-338.
54. Takahashi K, Yasuhara T, Shingo T, Muraoka K, Kameda M, Takeuchi A, Yano A, Kurozumi K, Agari T, Miyoshi Y, Kinugasa K, Date I (2008) Embryonic neural stem cells transplanted in middle cerebral artery occlusion model of rats demonstrated potent therapeutic effects, compared to adult neural stem cells. Brain Res 1234: 172-182.
55. Tambuyzer BR, Bergwerf I, De Vocht N, Reekmans K, Daans J, Jorens PG, Goossens H, Ysebaert DK, Chatterjee S, Van Marck E, Berneman ZN, Ponsaerts P. (2009) Allogeneic stromal cell implantation in brain tissue leads to robust microglial activation. Immunol Cell Biol 87: 267-273.
56. van der Stelt M, Veldhuis WB, van Haaften GW, Fezza F, Bisogno T, Bar PR, Veldink GA, Vliegenthart JF, Di Marzo V, Nicolay K (2001) Exogenous anandamide protects rat brain against acute neuronal injury in vivo. J Neurosci 21: 8765-8771.
57. Veldhuis WB, Floris S, van der Meide PH, Vos IM, de Vries HE, Dijkstra CD, Bär PR, Nicolay K (2003a) Interferonbeta prevents cytokine-induced neutrophil infiltration and attenuates blood-brain barrier disruption. J Cereb Blood Flow Metab 23: 1029-1039.
58. Veldhuis WB, van der Stelt M, Wadman MW, van Zadelhoff G, Maccarrone M, Fezza F, Veldink GA, Vliegenthart JF, Bär PR, Nicolay K, Di Marzo V (2003b) Neuroprotection by the endogenous cannabinoid anandamide and arvanil against in vivo excitotoxicity in the rat: role of vanilloid receptors and lipoxygenases. J Neurosci 23: 4127-4133.
59. Vendrame M, Cassady J, Newcomb J, Butler T, Pennypacker KR, Zigova T, Sanberg CD, Sanberg PR, Willing AE (2004) Infusion of human umbilical cord blood cells in a rat model of stroke dose-dependently rescues behavioral deficits and reduces infarct volume. Stroke 35: 2390-2395.
60. Walczak P, Chen N, Hudson JE, Willing AE, Garbuzova-Davis SN, Song S, Sanberg PR, Sanchez-Ramos J, Bickford PC, Zigova T. (2004) Do hematopoietic cells exposed to a neurogenic environment mimic properties of endogenous neural precursors? J Neurosci Res 76: 244-254.
61. Walczak P, Chen N, Eve D, Hudson J, Zigova T, Sanchez-Ramos J, Sanberg PR, Sanberg CD, Willing AE (2007) Long-term cultured human umbilical cord neural-like cells transplanted into the striatum of NOD SCID mice. Brain Res Bull 74: 155-163.
62. Wechsler LR, Kondziolka D (2003) Cell therapy: replacement. Stroke 34: 2081-2082.
63. Willing AE, Lixian J, Milliken M, Poulos S, Zigova T, Song S, Hart C, Sanchez-Ramos J, Sanberg PR (2003) Intravenous versus intrastriatal cord blood administration in a rodent model of stroke. J Neurosci Res 73: 296-307.
64. Wood MJ, Sloan DJ, Wood KJ, Charlton HM (1996) Indefinite survival of neural xenografts induced with anti-CD4 monoclonal antibodies. Neuroscience 70: 775-789.
65. Zhao Y, Marín O, Hermesz E, Powell A, Flames N, Palkovits M, Rubenstein JL, Westphal H (2003) The LIM-homeobox gene Lhx8 is required for the development of many cholinergic neurons in the mouse forebrain. Proc Natl Acad Sci U S A 100: 9005-9010.
66. Zigova T, Song S, Willing AE, Hudson JE, Newman MB, Saporta S, Sanchez-Ramos J, Sanberg PR (2002) Human umbilical cord blood cells express neural antigens after transplantation into the developing rat brain. Cell Transplant 11: 265-274.
67. Zychowicz M, Mehn D, Ruiz A, Frontczak-Baniewicz M, Rossi F, Buzanska L (2012) Patterning of human cord blood-derived stem cells on single cell posts and lines: Implications for neural commitment. Acta Neurobiol Exp (Wars) 72: 325-336.