Cellular replacement and regenerative medicine therapies in ischemic stroke

Papers of special note have been highlighted as: ▪ of interest ▪▪ of considerable interest

References

• 1  Bacigaluppi M, Comi G, Hermann DM. Animal models of ischemic stroke. Part two: modeling cerebral ischemia. Open Neurol. J.4,34–38 (2010).
  MedlineGoogle Scholar
• 2  Deb P, Sharma S, Hassan KM. Pathophysiologic mechanisms of acute ischemic stroke: an overview with emphasis on therapeutic significance beyond thrombolysis. Pathophysiology17(3),197–218 (2010).
  Medline CASGoogle Scholar
• 3  The Nervous System – Basic Science and Clinical Conditions. Michael-Titus A, Revest P, Shortland P (Eds). Churchill Livingstone, NY, USA, 217–243 (2007).
  Google Scholar
• 4  Banerjee DS. Stem cells in stroke. Presented at: Symposium in Stem Cell Repair and Regeneration. London, UK, 8 November 2010.
  Google Scholar
• 5  Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJ. Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet367(9524),1747–1757 (2006).
  MedlineGoogle Scholar
• 6  Albers GW, Bates VE, Clark WM, Bell R, Verro P, Hamilton SA. Intravenous tissue-type plasminogen activator for treatment of acute stroke: the Standard Treatment with Alteplase to Reverse Stroke (STARS) study. JAMA283(9),1145–1150 (2000).
  Medline CASGoogle Scholar
• 7  Alberts MJ. Hyperacute stroke therapy with tissue plasminogen activator. Am. J. Cardiol.80(4C),29D–34D (1997); discussion 35D–39D (1997).
  Medline CASGoogle Scholar
• 8  Cohen JE, Itshayek E, Moskovici S et al. State-of-the-art reperfusion strategies for acute ischemic stroke. J. Clin. Neurosci.18(3),319–323 (2011).
  MedlineGoogle Scholar
• 9  Chen ZM, Sandercock P, Pan HC et al. Indications for early aspirin use in acute ischemic stroke: a combined analysis of 40 000 randomized patients from the Chinese Acute Stroke Trial and the International Stroke Trial. On behalf of the CAST and IST collaborative groups. Stroke31(6),1240–1249 (2000).
  Medline CASGoogle Scholar
• 10  Ansara AJ, Nisly SA, Arif SA, Koehler JM, Nordmeyer ST. Aspirin dosing for the prevention and treatment of ischemic stroke: an indication-specific review of the literature. Ann. Pharmacother.44(5),851–862 (2010).
  Medline CASGoogle Scholar
• 11  Marsh JD, Keyrouz SG. Stroke prevention and treatment. J. Am. Coll. Cardiol.56(9),683–691 (2010).
  MedlineGoogle Scholar
• 12  Bernstein RA, Passman R. Prevention of stroke in patients with high-risk atrial fibrillation. Curr. Neurol. Neurosci. Rep.10(1),34–39 (2010).
  MedlineGoogle Scholar
• 13  Bose A, Henkes H, Alfke K et al. The Penumbra System: a mechanical device for the treatment of acute stroke due to thromboembolism. AJNR Am. J. Neuroradiol.29(7),1409–1413 (2008).
  Medline CASGoogle Scholar
• 14  Smith WS, Sung G, Saver J et al. Mechanical thrombectomy for acute ischemic stroke: final results of the Multi MERCI Trial. Stroke39(4),1205–1212 (2008).
  MedlineGoogle Scholar
• 15  Smith WS, Sung G, Starkman S et al. Safety and efficacy of mechanical embolectomy in acute ischemic stroke: results of the MERCI trial. Stroke36(7),1432–1438 (2005).
  MedlineGoogle Scholar
• 16  Kang DH, Hwang YH, Kim YS, Park J, Kwon O, Jung C. Direct thrombus retrieval using the reperfusion catheter of the penumbra system: forced-suction thrombectomy in acute ischemic stroke. AJNR Am. J. Neuroradiol.32(2),283–287 (2011).
  MedlineGoogle Scholar
• 17  Bliss TM, Andres RH, Steinberg GK. Optimizing the success of cell transplantation therapy for stroke. Neurobiol. Dis.37(2),275–283 (2010).
  MedlineGoogle Scholar
• 18  Lo EH, Dalkara T, Moskowitz MA. Mechanisms, challenges and opportunities in stroke. Nat. Rev. Neurosci.4(5),399–415 (2003).
  Medline CASGoogle Scholar
• 19  Savitz SI, Dinsmore JH, Wechsler LR, Rosenbaum DM, Caplan LR. Cell therapy for stroke. NeuroRx1(4),406–414 (2004).
  MedlineGoogle Scholar
• 20  Veizovic T, Beech JS, Stroemer RP, Watson WP, Hodges H. Resolution of stroke deficits following contralateral grafts of conditionally immortal neuroepithelial stem cells. Stroke32(4),1012–1019 (2001).
  Medline CASGoogle Scholar
• 21  Taguchi A, Soma T, Tanaka H et al. Administration of CD34⁺ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J. Clin. Invest.114(3),330–338 (2004).▪ Demonstrates the benefit of CD34+ cell implantation in mouse models, suggesting an essential role of CD34+ cells in angiogeneisis and neuronal regeneration.
  Medline CASGoogle Scholar
• 22  Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, Studer L. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol.27(3),275–280 (2009).▪▪ Shows an efficient method of directing human embryonic stem and induced pluripotent stem cells towards a neuronal lineage. This paper builds upon a number of neuronal differentiation publications.
  Medline CASGoogle Scholar
• 23  Reubinoff BE, Itsykson P, Turetsky T et al. Neural progenitors from human embryonic stem cells. Nat. Biotechnol.19(12),1134–1140 (2001).
  Medline CASGoogle Scholar
• 24  Zhang SC, Wernig M, Duncan ID, Brüstle O, Thomson JA. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol.19(12),1129–1133 (2001).
  Medline CASGoogle Scholar
• 25  Friling S, Andersson E, Thompson LH et al. Efficient production of mesencephalic dopamine neurons by Lmx1a expression in embryonic stem cells. Proc. Natl Acad. Sci. USA106(18),7613–7618 (2009).
  Medline CASGoogle Scholar
• 26  Andrews PW, Damjanov I, Simon D et al. Pluripotent embryonal carcinoma clones derived from the human teratocarcinoma cell line Tera-2. Differentiation in vivo and in vitro. Lab. Invest.50(2),147–162 (1984).
  Medline CASGoogle Scholar
• 27  Wertkin AM, Turner RS, Pleasure SJ et al. Human neurons derived from a teratocarcinoma cell line express solely the 695-amino acid amyloid precursor protein and produce intracellular beta-amyloid or A4 peptides. Proc. Natl Acad. Sci. USA90(20),9513–9517 (1993).
  Medline CASGoogle Scholar
• 28  Pleasure SJ, Lee VM. NTera 2 cells: a human cell line which displays characteristics expected of a human committed neuronal progenitor cell. J. Neurosci. Res.35(6),585–602 (1993).
  Medline CASGoogle Scholar
• 29  Pleasure SJ, Page C, Lee VM. Pure, postmitotic, polarized human neurons derived from NTera 2 cells provide a system for expressing exogenous proteins in terminally differentiated neurons. J. Neurosci.12(5),1802–1815 (1992).
  Medline CASGoogle Scholar
• 30  Pfisterer U, Wood J, Nihlberg K et al. Efficient induction of functional neurons from adult human fibroblasts. Cell Cycle10(19),3311–3316 (2011).
  Medline CASGoogle Scholar
• 31  Sanchez-Ramos J, Song S, Cardozo-Pelaez F et al. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp. Neurol.164(2),247–256 (2000).
  Medline CASGoogle Scholar
• 32  Kang SK, Lee DH, Bae YC, Kim HK, Baik SY, Jung JS. Improvement of neurological deficits by intracerebral transplantation of human adipose tissue-derived stromal cells after cerebral ischemia in rats. Exp. Neurol.183(2),355–366 (2003).
  Medline CASGoogle Scholar
• 33  Schwarting S, Litwak S, Hao W, Bahr M, Weise J, Neumann H. Hematopoietic stem cells reduce postischemic inflammation and ameliorate ischemic brain injury. Stroke39(10),2867–2875 (2008).
  Medline CASGoogle Scholar
• 34  Shyu W-C, Lin S-Z, Yang H-I et al. Functional recovery of stroke rats induced by granulocyte colony-stimulating factor-stimulated stem cells. Circulation110(13),1847–1854 (2004).
  Medline CASGoogle Scholar
• 35  Fasano CA, Chambers SM, Lee G, Tomishima MJ, Studer L. Efficient derivation of functional floor plate tissue from human embryonic stem cells. Cell Stem Cell6(4),336–347 (2010).
  Medline CASGoogle Scholar
• 36  Trounson A, Thakar RG, Lomax G, Gibbons D. Clinical trials for stem cell therapies. BMC Med.9,52 (2011).
  MedlineGoogle Scholar
• 37  Vazin T, Freed WJ. Human embryonic stem cells: derivation, culture, and differentiation: a review. Restor. Neurol. Neurosci.28(4),589–603 (2010).
  Medline CASGoogle Scholar
• 38  Cho KJ, Trzaska KA, Greco SJ et al. Neurons derived from human mesenchymal stem cells show synaptic transmission and can be induced to produce the neurotransmitter substance P by interleukin-1 alpha. Stem Cells23(3),383–391 (2005).
  Medline CASGoogle Scholar
• 39  Choong PF, Mok PL, Cheong SK, Leong CF, Then KY. Generating neuron-like cells from BM-derived mesenchymal stromal cells in vitro. Cytotherapy9(2),170–183 (2007).
  Medline CASGoogle Scholar
• 40  Guillemain I, Alonso G, Patey G, Privat A, Chaudieu I. Human NT2 neurons express a large variety of neurotransmission phenotypes in vitro. J. Comp. Neurol.422(3),380–395 (2000).
  Medline CASGoogle Scholar
• 41  Younkin DP, Tang CM, Hardy M et al. Inducible expression of neuronal glutamate receptor channels in the NT2 human cell line. Proc. Natl Acad. Sci. USA90(6),2174–2178 (1993).
  Medline CASGoogle Scholar
• 42  Neelands TR, King AP, Macdonald RL. Functional expression of L-, N-, P/Q-, and R-type calcium channels in the human NT2-N cell line. J. Neurophysiol.84(6),2933–2944 (2000).
  Medline CASGoogle Scholar
• 43  Trojanowski JQ, Mantione JR, Lee JH et al. Neurons derived from a human teratocarcinoma cell line establish molecular and structural polarity following transplantation into the rodent brain. Exp. Neurol.122(2),283–294 (1993).
  Medline CASGoogle Scholar
• 44  Woodbury D, Schwarz EJ, Prockop DJ, Black IB. Adult rat and human bone marrow stromal cells differentiate into neurons. J. Neurosci. Res.61(4),364–370 (2000).
  Medline CASGoogle Scholar
• 45  Deng W, Obrocka M, Fischer I, Prockop DJ. In vitro differentiation of human marrow stromal cells into early progenitors of neural cells by conditions that increase intracellular cyclic AMP. Biochem. Biophys. Res. Commun.282(1),148–152 (2001).
  Medline CASGoogle Scholar
• 46  Hermann A, Gastl R, Liebau S et al. Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J. Cell Sci.117(Pt 19),4411–4422 (2004).
  Medline CASGoogle Scholar
• 47  Pfisterer U, Kirkeby A, Torper O et al. Direct conversion of human fibroblasts to dopaminergic neurons. Proc. Natl Acad. Sci. USA108(25),10343–10348 (2011).▪ Demonstrates the potential of forced gene expression for converting fibroblasts into a neuronal lineage.
  Medline CASGoogle Scholar
• 48  Andrews PW. Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev. Biol.103(2),285–293 (1984).
  Medline CASGoogle Scholar
• 49  Bliss TM, Kelly S, Shah AK et al. Transplantation of hNT neurons into the ischemic cortex: cell survival and effect on sensorimotor behavior. J. Neurosci. Res.83(6),1004–1014 (2006).
  Medline CASGoogle Scholar
• 50  Kleppner SR, Robinson KA, Trojanowski JQ, Lee VM. Transplanted human neurons derived from a teratocarcinoma cell line (NTera-2) mature, integrate, and survive for over 1 month in the nude mouse brain. J. Comp. Neurol.357(4),618–632 (1995).
  Medline CASGoogle Scholar
• 51  Miyazono M, Lee VM, Trojanowski JQ. Proliferation, cell death, and neuronal differentiation in transplanted human embryonal carcinoma (NTera2) cells depend on the graft site in nude and severe combined immunodeficient mice. Lab. Invest.73(2),273–283 (1995).
  Medline CASGoogle Scholar
• 52  Pedersen ED, Aass HC, Rootwelt T, Fung M, Lambris JD, Mollnes TE. CD59 efficiently protects human NT2-N neurons against complement-mediated damage. Scand. J. Immunol.66(2–3),345–351 (2007).
  Medline CASGoogle Scholar
• 53  Yang LB, Li R, Meri S, Rogers J, Shen Y. Deficiency of complement defense protein CD59 may contribute to neurodegeneration in Alzheimer’s disease. J. Neurosci.20(20),7505–7509 (2000).
  Medline CASGoogle Scholar
• 54  Chen J, Li Y, Wang L et al. Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke32(4),1005–1011 (2001).
  Medline CASGoogle Scholar
• 55  Chen J, Li Y, Wang L, Lu M, Zhang X, Chopp M. Therapeutic benefit of intracerebral transplantation of bone marrow stromal cells after cerebral ischemia in rats. J. Neurol. Sci.189(1–2),49–57 (2001).
  Medline CASGoogle Scholar
• 56  Shen LH, Li Y, Chen J et al. Therapeutic benefit of bone marrow stromal cells administered 1 month after stroke. J. Cereb. Blood Flow Metab.27(1),6–13 (2007).
  MedlineGoogle Scholar
• 57  Sheridan WP, Fox RM, Begley CG et al. Effect of peripheral-blood progenitor cells mobilised by filgrastim (G-CSF) on platelet recovery after high-dose chemotherapy. Lancet339(8794),640–644 (1992).
  Medline CASGoogle Scholar
• 58  Petit I, Szyper-Kravitz M, Nagler A et al. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat. Immunol.3(7),687–694 (2002).
  Medline CASGoogle Scholar
• 59  Burns TC, Verfaillie CM, Low WC. Stem cells for ischemic brain injury: a critical review. J. Comp. Neurol.515(1),125–144 (2009).
  MedlineGoogle Scholar
• 60  Du HW, Liu N, Wang JH, Zhang YX, Chen RH, Xiao YC. [The effects of adipose-derived stem cell transplantation on the expression of IL-10 and TNF-α after cerebral ischaemia in rats.]. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi25(11),998–1001 (2009).
  Medline CASGoogle Scholar
• 61  Kelly S, Bliss TM, Shah AK et al. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc. Natl Acad. Sci. USA101(32),11839–11844 (2004).
  Medline CASGoogle Scholar
• 62  Darsalia V, Kallur T, Kokaia Z. Survival, migration and neuronal differentiation of human fetal striatal and cortical neural stem cells grafted in stroke-damaged rat striatum. Eur. J. Neurosci.26(3),605–614 (2007).
  MedlineGoogle Scholar
• 63  Nelson PT, Kondziolka D, Wechsler L et al. Clonal human (hNT) neuron grafts for stroke therapy: neuropathology in a patient 27 months after implantation. Am. J. Pathol.160(4),1201–1206 (2002).
  MedlineGoogle Scholar
• 64  Kondziolka D, Steinberg GK, Wechsler L et al. Neurotransplantation for patients with subcortical motor stroke: a Phase 2 randomized trial. J. Neurosurg.103(1),38–45 (2005).
  MedlineGoogle Scholar
• 65  Hara K, Yasuhara T, Maki M et al. Neural progenitor NT2N cell lines from teratocarcinoma for transplantation therapy in stroke. Prog. Neurobiol.85(3),318–334 (2008).
  Medline CASGoogle Scholar
• 66  Bang OY, Lee JS, Lee PH, Lee G. Autologous mesenchymal stem cell transplantation in stroke patients. Ann. Neurol.57(6),874–882 (2005).
  MedlineGoogle Scholar
• 67  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 Cells28(6),1099–1106 (2010).
  MedlineGoogle Scholar
• 68  Suárez-Monteagudo C, Hernandez-Ramirez P, Alvarez-Gonzalez L et al. Autologous bone marrow stem cell neurotransplantation in stroke patients. An open study. Restor. Neurol. Neurosci.27(3),151–161 (2009).
  MedlineGoogle Scholar
• 69  Savitz SI, Misra V, Kasam M et al. Intravenous autologous bone marrow mononuclear cells for ischemic stroke. Ann. Neurol.70(1),59–69 (2011).
  MedlineGoogle Scholar
• 70  Banerjee S, Williamson D, Habib N, Gordon M, Chataway J. Human stem cell therapy in ischaemic stroke: a review. Age Ageing40(1),7–13 (2010).
  MedlineGoogle Scholar
• 71  Wise J. Stroke patients take part in ‘milestone’ UK trial of stem cell therapy. BMJ341,C6574 (2010).
  MedlineGoogle Scholar
• 101  ReNeuron. ReNeuron receives UK ethics committee favourable opinion for stroke clinical trial. www.reneuron.com/press-release/reneuron-receives-uk-ethics-committee-favourable-opinion-for-stroke-clinical-trial-30-07-09
  Google Scholar