Vector-Free and Transgene-Free Human iPS Cells Differentiate into Functional Neurons and Enhance Functional Recovery after Ischemic Stroke in Mice

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Mohamad, Osama ^a   Drury Stewart, Danielle ^b   Song, Mingke ^a   Faulkner, Ben ^a   Chen, Dongdong ^a   Yu, Shan Ping ^a   Wei, Ling ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; MICROTUBULE ASSOCIATED PROTEIN 2; NESTIN; NEUROFILAMENT L PROTEIN; NEURON SPECIFIC NUCLEAR PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN TUJ1; SYNAPSIN I; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CELL FUNCTION; CELL MATURATION; CELL STRUCTURE; CONTROLLED STUDY; CONVALESCENCE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; STEM CELL TRANSPLANTATION; THERAPY EFFECT;

ACTION POTENTIALS; ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; CULTURE MEDIA, SERUM-FREE; EYE PROTEINS; GENETIC VECTORS; HOMEODOMAIN PROTEINS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; INFARCTION, MIDDLE CEREBRAL ARTERY; MICE; MICE, INBRED C57BL; NESTIN; NEURONS; PAIRED BOX TRANSCRIPTION FACTORS; PSYCHOMOTOR PERFORMANCE; RECOVERY OF FUNCTION; REGIONAL BLOOD FLOW; REPRESSOR PROTEINS; TRANSGENES;

EID: 84878133957     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064160     Document Type: Article

References (77)

1. Abdallah BM, Boissy P, Tan Q, Dahlgaard J, Traustadottir GA, et al. (2007) dlk1/FA1 regulates the function of human bone marrow mesenchymal stem cells by modulating gene expression of pro-inflammatory cytokines and immune response-related factors. J Biol Chem 282: 7339-7351.
2. Green AR, (2004) Protecting the brain: the search for a clinically effective neuroprotective drug for stroke. Crit Rev Neurobiol 16: 91-97.
3. Marler JR, (2007) NINDS clinical trials in stroke: lessons learned and future directions. Stroke 38: 3302-3307.
4. Bjorklund A, Lindvall O, (2000) Cell replacement therapies for central nervous system disorders. Nat Neurosci 3: 537-544.
5. Wei L, Cui L, Snider BJ, Rivkin M, Yu SS, et al. (2005) Transplantation of embryonic stem cells overexpressing Bcl-2 promotes functional recovery after transient cerebral ischemia. Neurobiol Dis 19: 183-193.
6. Hicks AU, Lappalainen RS, Narkilahti S, Suuronen R, Corbett D, et al. (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.
7. de Wert G, Mummery C, (2003) Human embryonic stem cells: research, ethics and policy. Hum Reprod 18: 672-682.
8. Takahashi K, Yamanaka S, (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
9. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, et al. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
10. Meissner A, Wernig M, Jaenisch R, (2007) Direct reprogramming of genetically unmodified fibroblasts into pluripotent stem cells. Nat Biotechnol 25: 1177-1181.
11. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, et al. (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448: 318-324.
12. Hu BY, Weick JP, Yu J, Ma LX, Zhang XQ, et al. (2010) Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc Natl Acad Sci U S A 107: 4335-4340.
13. Kim DS, Lee JS, Leem JW, Huh YJ, Kim JY, et al. (2010) Robust enhancement of neural differentiation from human ES and iPS cells regardless of their innate difference in differentiation propensity. Stem Cell Rev 6: 270-281.
14. Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, et al. (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27: 275-280.
15. Dimos JT, Rodolfa KT, Niakan KK, Weisenthal LM, Mitsumoto H, et al. (2008) Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321: 1218-1221.
16. Ebert AD, Yu J, Rose FF Jr, Mattis VB, Lorson CL, et al. (2009) Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 457: 277-280.
17. Hu BY, Zhang SC, (2009) Differentiation of spinal motor neurons from pluripotent human stem cells. Nat Protoc 4: 1295-1304.
18. Karumbayaram S, Novitch BG, Patterson M, Umbach JA, Richter L, et al. (2009) Directed differentiation of human-induced pluripotent stem cells generates active motor neurons. Stem Cells 27: 806-811.
19. Lee G, Papapetrou EP, Kim H, Chambers SM, Tomishima MJ, et al. (2009) Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 461: 402-406.
20. Soldner F, Hockemeyer D, Beard C, Gao Q, Bell GW, et al. (2009) Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 136: 964-977.
21. Wernig M, Zhao JP, Pruszak J, Hedlund E, Fu D, et al. (2008) Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proc Natl Acad Sci U S A 105: 5856-5861.
22. Huangfu D, Osafune K, Maehr R, Guo W, Eijkelenboom A, et al. (2008) Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol 26: 1269-1275.
23. Gonzalez F, Barragan Monasterio M, Tiscornia G, Montserrat Pulido N, Vassena R, et al. (2009) Generation of mouse-induced pluripotent stem cells by transient expression of a single nonviral polycistronic vector. Proc Natl Acad Sci U S A 106: 8918-8922.
24. Kaji K, Norrby K, Paca A, Mileikovsky M, Mohseni P, et al. (2009) Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature 458: 771-775.
25. Lin T, Ambasudhan R, Yuan X, Li W, Hilcove S, et al. (2009) A chemical platform for improved induction of human iPSCs. Nat Methods 6: 805-888.
26. Maherali N, Ahfeldt T, Rigamonti A, Utikal J, Cowan C, et al. (2008) A high-efficiency system for the generation and study of human induced pluripotent stem cells. Cell Stem Cell 3: 340-345.
27. Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S, (2008) Generation of mouse induced pluripotent stem cells without viral vectors. Science 322: 949-953.
28. Yusa K, Rad R, Takeda J, Bradley A, (2009) Generation of transgene-free induced pluripotent mouse stem cells by the piggyBac transposon. Nat Methods 6: 363-369.
29. Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, et al. (2009) Human induced pluripotent stem cells free of vector and transgene sequences. Science 324: 797-801.
30. Ludwig TE, Levenstein ME, Jones JM, Berggren WT, Mitchen ER, et al. (2006) Derivation of human embryonic stem cells in defined conditions. Nat Biotechnol 24: 185-187.
31. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
32. Drury-Stewart D, Song M, Mohamad O, Yu SP, Wei L, (2011) Small molecule promoted feeder free and adherent differentiation of functional neurons from human embryonic and induced pluripotent stem cells Journal of Stem Cells. 6: 1.
33. Manzerra P, Behrens MM, Canzoniero LM, Wang XQ, Heidinger V, et al. (2001) Zinc induces a Src family kinase-mediated up-regulation of NMDA receptor activity and excitotoxicity. Proc Natl Acad Sci U S A 98: 11055-11061.
34. Wei L, Rovainen CM, Woolsey TA, (1995) Ministrokes in rat barrel cortex. Stroke 26: 1459-1462.
35. Mohamad O, Chen D, Zhang L, Hofmann C, Wei L, et al. (2011) Erythropoietin reduces neuronal cell death and hyperalgesia induced by peripheral inflammatory pain in neonatal rats. Mol Pain 7: 51.
36. Wei L, Yu SP, Gottron F, Snider BJ, Zipfel GJ, et al. (2003) Potassium channel blockers attenuate hypoxia- and ischemia-induced neuronal death in vitro and in vivo. Stroke 34: 1281-1286.
37. Wei N, Yu SP, Gu X, Taylor TM, Song D, et al. (2012) Delayed Intranasal Delivery of Hypoxic-preconditioned Bone Marrow Mesenchymal Stem Cells Enhanced Cell Homing and Therapeutic Benefits after Ischemic Stroke in Mice. Cell Transplant.
38. Kode JA, Mukherjee S, Joglekar MV, Hardikar AA, (2009) Mesenchymal stem cells: immunobiology and role in immunomodulation and tissue regeneration. Cytotherapy 11: 377-391.
39. Choi KE, Hall CL, Sun JM, Wei L, Mohamad O, et al. (2012) A novel stroke therapy of pharmacologically induced hypothermia after focal cerebral ischemia in mice. FASEB J 26: 2799-2810.
40. Li Y, Yu SP, Mohamad O, Genetta T, Wei L, (2010) Sublethal transient global ischemia stimulates migration of neuroblasts and neurogenesis in mice. Transl Stroke Res 1: 184-196.
41. Schmitz C, Hof PR, (2005) Design-based stereology in neuroscience. Neuroscience 130: 813-831.
42. Freret T, Bouet V, Leconte C, Roussel S, Chazalviel L, et al. (2009) Behavioral deficits after distal focal cerebral ischemia in mice: Usefulness of adhesive removal test. Behav Neurosci 123: 224-230.
43. Martin MJ, Muotri A, Gage F, Varki A, (2005) Human embryonic stem cells express an immunogenic nonhuman sialic acid. Nat Med 11: 228-232.
44. Zhang SC, Wernig M, Duncan ID, Brustle O, Thomson JA, (2001) In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19: 1129-1133.
45. Schulz TC, Palmarini GM, Noggle SA, Weiler DA, Mitalipova MM, et al. (2003) Directed neuronal differentiation of human embryonic stem cells. BMC Neurosci 4: 27.
46. Gerrard L, Rodgers L, Cui W, (2005) Differentiation of human embryonic stem cells to neural lineages in adherent culture by blocking bone morphogenetic protein signaling. Stem Cells 23: 1234-1241.
47. Ingvarsson S, (1990) The myc gene family proteins and their role in transformation and differentiation. Semin Cancer Biol 1: 359-369.
48. Yamashita T, Kawai H, Tian F, Ohta Y, Abe K, (2011) Tumorigenic development of induced pluripotent stem cells in ischemic mouse brain. Cell Transplant 20: 883-891.
49. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, et al. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147.
50. Kawasaki H, Mizuseki K, Nishikawa S, Kaneko S, Kuwana Y, et al. (2000) Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28: 31-40.
51. Lee H, Shamy GA, Elkabetz Y, Schofield CM, Harrsion NL, et al. (2007) Directed differentiation and transplantation of human embryonic stem cell-derived motoneurons. Stem Cells 25: 1931-1939.
52. Hu BY, Weick JP, Yu J, Ma LX, Zhang XQ,et al. Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc Natl Acad Sci U S A 107: 4335-4340.
53. Kim DS, Lee JS, Leem JW, Huh YJ, Kim JY,et al. Robust enhancement of neural differentiation from human ES and iPS cells regardless of their innate difference in differentiation propensity. Stem Cell Rev 6: 270-281.
54. Ishibashi S, Sakaguchi M, Kuroiwa T, Yamasaki M, Kanemura Y, et al. (2004) Human neural stem/progenitor cells, expanded in long-term neurosphere culture, promote functional recovery after focal ischemia in Mongolian gerbils. J Neurosci Res 78: 215-223.
55. Kelly S, Bliss TM, Shah AK, Sun GH, Ma M, et al. (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.
56. Theus MH, Wei L, Cui L, Francis K, Hu X, et al. (2008) In vitro hypoxic preconditioning of embryonic stem cells as a strategy of promoting cell survival and functional benefits after transplantation into the ischemic rat brain. Exp Neurol 210: 656-670.
57. Hu X, Wei L, Taylor TM, Wei J, Zhou X, et al. (2011) Hypoxic preconditioning enhances bone marrow mesenchymal stem cell migration via Kv2.1 channel and FAK activation. Am J Physiol Cell Physiol 301: C362-372.
58. Francis KR, Wei L, (2010) Human embryonic stem cell neural differentiation and enhanced cell survival promoted by hypoxic preconditioning. Cell Death Dis 1: e22.
59. Ziv Y, Avidan H, Pluchino S, Martino G, Schwartz M, (2006) Synergy between immune cells and adult neural stem/progenitor cells promotes functional recovery from spinal cord injury. Proc Natl Acad Sci U S A 103: 13174-13179.
60. Ziv Y, Ron N, Butovsky O, Landa G, Sudai E, et al. (2006) Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 9: 268-275.
61. Beers DR, Henkel JS, Zhao W, Wang J, Appel SH, (2008) CD4+ T cells support glial neuroprotection, slow disease progression, and modify glial morphology in an animal model of inherited ALS. Proc Natl Acad Sci U S A 105: 15558-15563.
62. Chiu IM, Chen A, Zheng Y, Kosaras B, Tsiftsoglou SA, et al. (2008) T lymphocytes potentiate endogenous neuroprotective inflammation in a mouse model of ALS. Proc Natl Acad Sci U S A 105: 17913-17918.
63. Ben-Hur T, Ben-Menachem O, Furer V, Einstein O, Mizrachi-Kol R, et al. (2003) Effects of proinflammatory cytokines on the growth, fate, and motility of multipotential neural precursor cells. Mol Cell Neurosci 24: 623-631.
64. Dunn GP, Old LJ, Schreiber RD, (2004) The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21: 137-148.
65. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD, (2002) Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 3: 991-998.
66. Marcen R, (2009) Immunosuppressive drugs in kidney transplantation: impact on patient survival, and incidence of cardiovascular disease, malignancy and infection. Drugs 69: 2227-2243.
67. Oki K, Tatarishvili J, Wood J, Koch P, Wattananit S, et al. (2012) Human-induced pluripotent stem cells form functional neurons and improve recovery after grafting in stroke-damaged brain. Stem Cells 30: 1120-1133.
68. Jensen MB, Yan H, Krishnaney-Davison R, Al Sawaf A, Zhang SC (2011) Survival and Differentiation of Transplanted Neural Stem Cells Derived from Human Induced Pluripotent Stem Cells in A Rat Stroke Model. J Stroke Cerebrovasc Dis.
69. Jiang M, Lv L, Ji H, Yang X, Zhu W, et al. (2011) Induction of pluripotent stem cells transplantation therapy for ischemic stroke. Mol Cell Biochem 354: 67-75.
70. Kawai H, Yamashita T, Ohta Y, Deguchi K, Nagotani S, et al. (2010) Tridermal tumorigenesis of induced pluripotent stem cells transplanted in ischemic brain. J Cereb Blood Flow Metab 30: 1487-1493.
71. Chen SJ, Chang CM, Tsai SK, Chang YL, Chou SJ, et al. (2010) Functional improvement of focal cerebral ischemia injury by subdural transplantation of induced pluripotent stem cells with fibrin glue. Stem Cells Dev 19: 1757-1767.
72. Daadi MM, Maag AL, Steinberg GK, (2008) Adherent self-renewable human embryonic stem cell-derived neural stem cell line: functional engraftment in experimental stroke model. PLoS One 3: e1644.
73. Taguchi A, Soma T, Tanaka H, Kanda T, Nishimura H, et al. (2004) Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J Clin Invest 114: 330-338.
74. Blurton-Jones M, Kitazawa M, Martinez-Coria H, Castello NA, Muller FJ, et al. (2009) Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc Natl Acad Sci U S A 106: 13594-13599.
75. Ploughman M, Windle V, MacLellan CL, White N, Dore JJ, et al. (2009) Brain-derived neurotrophic factor contributes to recovery of skilled reaching after focal ischemia in rats. Stroke 40: 1490-1495.
76. Schabitz WR, Berger C, Kollmar R, Seitz M, Tanay E, et al. (2004) Effect of brain-derived neurotrophic factor treatment and forced arm use on functional motor recovery after small cortical ischemia. Stroke 35: 992-997.
77. Wei L, Fraser JL, Lu ZY, Hu X, Yu SP, (2012) Transplantation of hypoxia preconditioned bone marrow mesenchymal stem cells enhances angiogenesis and neurogenesis after cerebral ischemia in rats. Neurobiol Dis 46: 635-645.