Graft and host interactions following transplantation of neural stem cells to organotypic striatal cultures

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Bibliography

• 1  Snyder EY, Daley GQ, Goodell M: Taking stock and planning for the next decade: realistic prospects for stem cell therapies for the nervous system. J. Neurosci. Res.76(2),157–168 (2004).
  Medline CASGoogle Scholar
• 2  Singec I, Jandial R, Crain A, Nikkhah G, Snyder EY: The leading edge of stem cell therapeutics. Annu. Rev. Med.58,313–328 (2007).
  Medline CASGoogle Scholar
• 3  Lindvall O, Kokaia Z: Stem cells for the treatment of neurological disorders. Nature441(7097),1094–1096 (2006).
  Medline CASGoogle Scholar
• 4  Lindvall O, Kokaia Z: Stem cells in human neurodegenerative disorders – time for clinical translation?.. J. Clin. Invest.120(1),29–40 (2010).▪ Presents a recent review of the hype and hope of neural stem cell transplantation therapies.
  Medline CASGoogle Scholar
• 5  Lindvall O, Kokaia Z, Martinez-Serrano A: Stem cell therapy for human neurodegenerative disorders – how to make it work. Nat. Med.10(Suppl.),S42–S50 (2004).
  MedlineGoogle Scholar
• 6  Li J, Imitola J, Snyder EY, Sidman RL: Neural stem cells rescue nervous purkinje neurons by restoring molecular homeostasis of tissue plasminogen activator and downstream targets. J. Neurosci.26(30),7839–7848 (2006).▪ Shows that engrafted neural stem cells (NSCs) can rescue host cells by contact-dependent mechanisms.
  Medline CASGoogle Scholar
• 7  Madhavan L, Ourednik V, Ourednik J: Grafted neural stem cells shield the host environment from oxidative stress. Ann. NY Acad. Sci.1049,185–188 (2005).
  MedlineGoogle Scholar
• 8  Ourednik J, Ourednik V, Lynch WP, Schachner M, Snyder EY: Neural stem cells display an inherent mechanism for rescuing dysfunctional neurons. Nat. Biotechnol.20(11),1103–1110 (2002).▪▪ First clear evidence that the positive effects of NSC engraftment is in part attributed to rescue rather than replacement of host neurons. Thus, host structures may benefit not only from NSC-derived replacement of lost neurons, but also from the ‘chaperone’ effect of some NSC-derived progeny.
  Medline CASGoogle Scholar
• 9  Lee JP, Jeyakumar M, Gonzalez R et al.: Stem cells act through multiple mechanisms to benefit mice with neurodegenerative metabolic disease. Nat. Med.13(4),439–447 (2007).
  Medline CASGoogle Scholar
• 10  Redmond DE Jr, Bjugstad KB, Teng YD et al.: Behavioral improvement in a primate Parkinson’s model is associated with multiple homeostatic effects of human neural stem cells. Proc. Natl Acad. Sci. USA104(29),12175–12180 (2007).
  Medline CASGoogle Scholar
• 11  Jäderstad J, Jäderstad LM, Li J et al.: Communication via gap junctions underlies early functional and beneficial interactions between grafted neural stem cells and the host. Proc. Natl Acad. Sci. USA107(11),5184–5189 (2010).▪▪ Describes the pivotal mediation by gap-junctional coupling of some modulatory, homeostatic and protective actions on host systems as well as establishing a template for the subsequent development of electrochemical synaptic intercellular communication.
  MedlineGoogle Scholar
• 12  Parker MA, Anderson JK, Corliss DA et al.: Expression profile of an operationally-defined neural stem cell clone. Exp. Neurol.194(2),320–332 (2005).
  Medline CASGoogle Scholar
• 13  Snyder EY, Deitcher DL, Walsh C, Arnold-Aldea S, Hartwieg EA, Cepko CL: Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell68(1),33–51 (1992).▪ First description of the C17.2 neural stem cell line, which was utilized in the current study.
  Medline CASGoogle Scholar
• 14  Gahwiler BH: Organotypic monolayer cultures of nervous tissue. J. Neurosci. Methods4(4),329–342 (1981).
  Medline CASGoogle Scholar
• 15  Gahwiler BH: Organotypic cultures of neural tissue. Trends Neurosci.11(11),484–489 (1988).
  Medline CASGoogle Scholar
• 16  Gahwiler BH, Capogna M, Debanne D, Mckinney RA, Thompson SM: Organotypic slice cultures: a technique has come of age. Trends Neurosci.20(10),471–477 (1997).▪ Provides a comprehensive review of previous applications of the organotypic culture technique used in the current study.
  Medline CASGoogle Scholar
• 17  Thonabulsombat C, Johansson S, Spenger C, Ulfendahl M, Olivius P: Implanted embryonic sensory neurons project axons toward adult auditory brainstem neurons in roller drum and stoppini co-cultures. Brain Res.1170,48–58 (2007).
  Medline CASGoogle Scholar
• 18  Kimberley AB-H, Enrique A, Curt RF: Generation of tyrosine hydroxylase positive neurons from human embryonic stem cells after coculture with cellular substrates and exposure to gdnf. Stem Cells22(5),669–674 (2004).
  MedlineGoogle Scholar
• 19  Raffaqat MA, Maaløv CA, Kølvraa SL, Jens Z, Alberto M-S, Morten M: Dopaminergic differentiation of human neural stem cells mediated by co-cultured rat striatal brain slices. J. Neurochem.105(2),460–470 (2008).
  MedlineGoogle Scholar
• 20  Ostergaard K, Schou JP, Gahwiler BH, Zimmer J: Tyrosine hydroxylase immunoreactive neurons in organotypic slice cultures of the rat striatum and neocortex. Exp. Brain Res.83(2),357–365 (1991).
  Medline CASGoogle Scholar
• 21  Lu P, Jones LL, Snyder EY, Tuszynski MH: Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp. Neurol.181(2),115–129 (2003).
  Medline CASGoogle Scholar
• 22  Park KI, Himes BT, Stieg PE, Tessler A, Fischer I, Snyder EY: Neural stem cells may be uniquely suited for combined gene therapy and cell replacement: evidence from engraftment of neurotrophin-3-expressing stem cells in hypoxic-ischemic brain injury. Exp. Neurol.199(1),179–190 (2006).
  Medline CASGoogle Scholar
• 23  Brewer GJ: Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus. J. Neurosci. Res.42(5),674–683 (1995).
  Medline CASGoogle Scholar
• 24  Brewer GJ, Torricelli JR, Evege EK, Price PJ: Optimized survival of hippocampal neurons in B27-supplemented neurobasal, a new serum-free medium combination. J. Neurosci. Res.35(5),567–576 (1993).
  Medline CASGoogle Scholar
• 25  Flax JD, Aurora S, Yang C et al.: Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat. Biotechnol.16(11),1033–1039 (1998).
  Medline CASGoogle Scholar
• 26  Imitola J, Raddassi K, Park KI et al.: Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1a/CXC chemokine receptor 4 pathway. Proc. Natl Acad. Sci. USA101(52),18117–18122 (2004).
  Medline CASGoogle Scholar
• 27  Lothian C, Lendahl U: An evolutionarily conserved region in the second intron of the human nestin gene directs gene expression to CNS progenitor cells and to early neural crest cells. Eur. J. Neurosci.9(3),452–462 (1997).
  Medline CASGoogle Scholar
• 28  Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD: A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci.2(4),287–293 (2001).
  Medline CASGoogle Scholar
• 29  Snyder EY, Taylor RM, Wolfe JH: Neural progenitor cell engraftment corrects lysosomal storage throughout the MPS VII mouse brain. Nature374(6520),367–370 (1995).
  Medline CASGoogle Scholar
• 30  Park KI, Hack MA, Ourednik J et al.: Acute injury directs the migration, proliferation, and differentiation of solid organ stem cells: evidence from the effect of hypoxia-ischemia in the CNS on clonal “reporter” neural stem cells. Exp. Neurol.199(1),156–178 (2006).
  MedlineGoogle Scholar
• 31  Yandava BD, Billinghurst LL, Snyder EY: “Global” cell replacement is feasible via neural stem cell transplantation: evidence from the dysmyelinated shiverer mouse brain. Proc. Natl Acad. Sci. USA96(12),7029–7034 (1999).
  Medline CASGoogle Scholar
• 32  Rosario CM, Yandava BD, Kosaras B, Zurakowski D, Sidman RL, Snyder EY: Differentiation of engrafted multipotent neural progenitors towards replacement of missing granule neurons in meander tail cerebellum may help determine the locus of mutant gene action. Development124(21),4213–4224 (1997).
  Medline CASGoogle Scholar
• 33  Snyder EY, Yoon C, Flax JD, Macklis JD: Multipotent neural precursors can differentiate toward replacement of neurons undergoing targeted apoptotic degeneration in adult mouse neocortex. Proc. Natl Acad. Sci. USA94(21),11663–11668 (1997).
  Medline CASGoogle Scholar
• 34  Yan J, Welsh AM, Bora SH, Snyder EY, Koliatsos VE: Differentiation and tropic/trophic effects of exogenous neural precursors in the adult spinal cord. J. Comp. Neurol.480(1),101–114 (2004).
  MedlineGoogle Scholar
• 35  Teng YD, Lavik EB, Qu X et al.: Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc. Natl Acad. Sci. USA99(5),3024–3029 (2002).
  Medline CASGoogle Scholar
• 36  Benninger F, Beck H, Wernig M, Tucker KL, Brustle O, Scheffler B: Functional integration of embryonic stem cell-derived neurons in hippocampal slice cultures. J. Neurosci.23(18),7075–7083 (2003).
  Medline CASGoogle Scholar
• 37  Scheffler B, Schmandt T, Schroder W et al.: Functional network integration of embryonic stem cell-derived astrocytes in hippocampal slice cultures. Development130(22),5533–5541 (2003).
  Medline CASGoogle Scholar
• 38  Kamei N, Tanaka N, Oishi Y et al.: BDNF, NT-3, and NGF released from transplanted neural progenitor cells promote corticospinal axon growth in organotypic cocultures. Spine32(12),1272–1278 (2007).▪ Depicts glial network integration as a potential route for widespread transcellular delivery of small molecules to the CNS.
  MedlineGoogle Scholar
• 39  Gahwiler BH: Nerve cells in organotypic cultures. JAMA245(18),1858–1859 (1981).
  Medline CASGoogle Scholar
• 40  Mohajerani MH, Cherubini E: Spontaneous recurrent network activity in organotypic rat hippocampal slices. Eur. J. Neurosci.22(1),107–118 (2005).
  MedlineGoogle Scholar
• 41  Joannides AJ, Webber DJ, Raineteau O et al.: Environmental signals regulate lineage choice and temporal maturation of neural stem cells from human embryonic stem cells. Brain130(Pt 5),1263–1275 (2007).
  MedlineGoogle Scholar
• 42  Jäderstad J, Jäderstad LM, Herlenius E: Dynamic changes in connexin expression following engraftment of neural stem cells to striatal tissue. Exp. Cell Res. (2010) (Epub ahead of print).
  MedlineGoogle Scholar
• 43  Clarke DJ, Brundin P, Strecker RE, Nilsson OG, Bjorklund A, Lindvall O: Human fetal dopamine neurons grafted in a rat model of Parkinson’s disease: ultrastructural evidence for synapse formation using tyrosine hydroxylase immunocytochemistry. Exp. Brain Res.73(1),115–126 (1988).
  Medline CASGoogle Scholar
• 44  Takahashi J, Palmer TD, Gage FH: Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural stem cell cultures. J. Neurobiol.38(1),65–81 (1999).
  Medline CASGoogle Scholar
• 45  Yang Z, Watanabe M, Nishiyama A: Optimization of oligodendrocyte progenitor cell culture method for enhanced survival. J. Neurosci. Methods149(1),50–56 (2005).
  Medline CASGoogle Scholar
• 46  Xie C, Markesbery WR, Lovell MA: Survival of hippocampal and cortical neurons in a mixture of MEM⁺ and B27-supplemented neurobasal medium. Free Radic. Biol. Med.28(5),665–672 (2000).
  Medline CASGoogle Scholar
• 47  Kivell BM, Mcdonald FJ, Miller JH: Serum-free culture of rat post-natal and fetal brainstem neurons. Brain Res. Dev. Brain Res.120(2),199–210 (2000).
  Medline CASGoogle Scholar
• 48  Farso MC, Carroll FY, Beart PM: Establishment of primary cultures of rat olfactory bulb under serum-free conditions for studies of cellular injury. Cell Tissue Res.323(2),343–349 (2006).
  MedlineGoogle Scholar
• 49  Avossa D, Grandolfo M, Mazzarol F, Zatta M, Ballerini L: Early signs of motoneuron vulnerability in a disease model system: characterization of transverse slice cultures of spinal cord isolated from embryonic als mice. Neuroscience138(4),1179–1194 (2006).
  Medline CASGoogle Scholar
• 50  Adamchik Y, Frantseva MV, Weisspapir M, Carlen PL, Perez Velazquez JL: Methods to induce primary and secondary traumatic damage in organotypic hippocampal slice cultures. Brain Res. Brain Res. Protoc.5(2),153–158 (2000).
  Medline CASGoogle Scholar
• 51  Pekny M, Nilsson M: Astrocyte activation and reactive gliosis. Glia50(4),427–434 (2005).
  MedlineGoogle Scholar
• 52  Frisen J, Johansson CB, Torok C, Risling M, Lendahl U: Rapid, widespread, and longlasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J. Cell Biol.131(2),453–464 (1995).
  Medline CASGoogle Scholar
• 53  Takamiya Y, Kohsaka S, Toya S, Otani M, Tsukada Y: Immunohistochemical studies on the proliferation of reactive astrocytes and the expression of cytoskeletal proteins following brain injury in rats. Brain Res.466(2),201–210 (1988).
  Medline CASGoogle Scholar
• 54  Sofroniew MV: Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci.32(12),638–647 (2009).
  Medline CASGoogle Scholar
• 55  Park DH, Borlongan CV, Willing AE et al.: Human umbilical cord blood cell grafts for brain ischemia. Cell Transplant18(9),985–998 (2009).
  MedlineGoogle Scholar
• 56  Li L, Lundkvist A, Andersson D et al.: Protective role of reactive astrocytes in brain ischemia. J. Cereb. Blood Flow Metab.28(3),468–481 (2008).
  MedlineGoogle Scholar
• 57  Connor B, Dragunow M: The role of neuronal growth factors in neurodegenerative disorders of the human brain. Brain Res. Brain Res. Rev.27(1),1–39 (1998).
  Medline CASGoogle Scholar
• 58  Escandon E, Soppet D, Rosenthal A et al.: Regulation of neurotrophin receptor expression during embryonic and postnatal development. J. Neurosci.14(4),2054–2068 (1994).
  Medline CASGoogle Scholar
• 59  Jung AB, Bennett JP: Development of striatal dopaminergic function. III: pre- and postnatal development of striatal and cortical mRNAs for the neurotrophin receptors trkBTK⁺ and trkC and their regulation by synaptic dopamine. Brain Res. Dev. Brain Res.94(2),133–143 (1996).
  Medline CASGoogle Scholar
• 60  Lamballe F, Smeyne RJ, Barbacid M: Developmental expression of trkC, the neurotrophin-3 receptor, in the mammalian nervous system. J. Neurosci.14(1),14–28 (1994).
  Medline CASGoogle Scholar
• 61  Deierborg T, Soulet D, Roybon L, Hall V, Brundin P: Emerging restorative treatments for parkinson’s disease. Prog. Neurobiol.85(4),407–432 (2008).
  Medline CASGoogle Scholar
• 62  Ourednik V, Ourednik J: Graft/host relationships in the developing and regenerating cns of mammals. Ann. NY Acad. Sci.1049,172–184 (2005).
  MedlineGoogle Scholar
• 63  Jäderstad J, Danielsson LM, Ourednik V, Snyder EY, Herlenius E: Communication via gap junctions underlies early functional interactions between grafted neural stem cells and the host. Exp. Neurol.198(2),572 (2006).
  Google Scholar
• 64  Rela L, Bordey A, Greer CA: Olfactory ensheathing cell membrane properties are shaped by connectivity. Glia58(6),665–678 (2010).
  MedlineGoogle Scholar
• 65  Brundin P, Li J-Y, Holton JL, Lindvall O, Revesz T: Research in motion: the enigma of Parkinson’s disease pathology spread. Nat. Rev. Neurosci.9(10),741–745 (2008).
  Medline CASGoogle Scholar