DOI: https://doi.org/10.25305/unj.191943

Cell therapy in experimental TBI

Mykola I. Lisianyi

Abstract


The review of the literature deals with the results of the use of cell therapy in experimental TBI in animals, which analyses stem cells of different origin and degree of differentiation — neuronal embryonic, mesenchymal multipotent, totipotent blastogenic, endothelial cells and others.

The very first studies were conducted with neurogenic (nerve) stem cells (NSCs) and their progenitors, which were received from various brain structures of the embryo or adult animal. Most studies have been conducted using the mesenchymal stem cells (MSCs), due to the capacity of these cells to transform into nerve cells and endothelial cells. MSCs were obtained from various sources — adipose and bone tissue, placenta, umbilical cord or amniotic membrane and others.

The primary hypothesis was that transplanted stem cells were able to transform into neurons. Eventually, they were found to only secrete paracrine humoral factors that stimulate neuronal regeneration. It was established that the more stells were administered the more effective neuron restoration was. The stem cells were injected in various ways, mostly through stereotaxic or intravenous administration, although other methods were described, and cell introduction was either immediately after TBI or after 24 hours or several days. The accumulation of MSCs in the injured brain when administered intravenously was slight ranging from 1.4 % to 0.01  %, survival was short, regardless of the route of administration — to 14  % of cells within the week and only 0.6 % within a month. Today, there is no consensus about the mechanism of action of stem cells in TBI and there are at least six different hypotheses on this issue. The review also focuses on adult stem cells and the search for ways to activate and migrate them to the TBI injury zone, which may serve as one of the new approaches to treating the effects of TBI in humans.


Keywords


traumatic brain injury in animals; cell therapy; stem cells; transplantation

References


1. Maas AIR, Menon DK, Adelson PD, Andelic N, Bell MJ, Belli A, Bragge P, Brazinova A, Büki A, Chesnut RM, Citerio G, Coburn M, Cooper DJ, Crowder AT, Czeiter E, Czosnyka M, Diaz-Arrastia R, Dreier JP, Duhaime AC, Ercole A. Traumatic brain injury: integrated approaches to improve prevention, clinical care, and research. Lancet Neurol. 2017 Dec;16(12):987-1048. [CrossRef] [PubMed]

2. Zhou Y, Shao A, Xu W, Wu H, Deng Y. Advance of Stem Cell Treatment for Traumatic Brain Injury. Front Cell Neurosci. 2019 Aug; 13:301. [CrossRef] [PubMed] [PubMed Central]

3. Chayka AV, Zabenko YY, Labunets IF, Pivneva TA. Traumatic unjury: pathogenesis, experimental models, prospects of cell therapy. Cell and Organ Transplantology. 2017;5(2):209-215. [CrossRef]

4. Jain KK. Neuroprotection in traumatic brain injury. Drug Discov Today. 2008 Dec;13(23-24):1082-9. [CrossRef] [PubMed]

5. Umile EM, Sandel ME, Alavi A, Terry CM, Plotkin RC. Dynamic imaging in mild traumatic brain injury: support for the theory of medial temporal vulnerability. Arch Phys Med Rehabil. 2002 Nov;83(11):1506-13. [CrossRef] [PubMed]

6. Kelley BJ, Lifshitz J, Povlishock JT. Neuroinflammatory responses after experimental diffuse traumatic brain injury. J Neuropathol Exp Neurol. 2007 Nov;66(11):989-1001. [CrossRef] [PubMed]

7. Algattas H, Huang JH. Traumatic Brain Injury pathophysiology and treatments: early, intermediate, and late phases post-injury. Int J Mol Sci. 2013 Dec;15(1):309-41. [CrossRef] [PubMed] [PubMed Central]

8. Kotapka MJ, Graham DI, Adams JH, Gennarelli TA. Hippocampal pathology in fatal human head injury without high intracranial pressure. J Neurotrauma. 1994 Jun;11(3):317-24. [CrossRef] [PubMed]

9. Ugoya SO, Tu J. Bench to bedside of neural stem cell in traumatic brain injury. Stem Cells Int. 2012;2012:141624. [CrossRef] [PubMed] [PubMed Central]

10. Bedi SS, Walker PA, Shah SK, Jimenez F, Thomas CP, Smith P, Hetz RA, Xue H, Pati S, Dash PK, Cox CS Jr. Autologous bone marrow mononuclear cells therapy attenuates activated microglial/macrophage response and improves spatial learning after traumatic brain injury. J Trauma Acute Care Surg. 2013 Sep;75(3):410-6. [CrossRef] [PubMed] [PubMed Central]

11. Richardson RM, Singh A, Sun D, Fillmore HL, Dietrich DW 3rd, Bullock MR. Stem cell biology in traumatic brain injury: effects of injury and strategies for repair. J Neurosurg. 2010 May;112(5):1125-38. [CrossRef] [PubMed]

12. Molcanyi M, Riess P, Bentz K, Maegele M, Hescheler J, Schäfke B, Trapp T, Neugebauer E, Klug N, Schäfer U. Trauma-associated inflammatory response impairs embryonic stem cell survival and integration after implantation into injured rat brain. J Neurotrauma. 2007 Apr;24(4):625-37. [CrossRef] [PubMed]

13. Cox CS Jr. Cellular therapy for traumatic neurological injury. Pediatr Res. 2018 Jan;83(1-2):325-332. [CrossRef] [PubMed]

14. Riess P, Zhang C, Saatman KE, Laurer HL, Longhi LG, Raghupathi R, Lenzlinger PM, Lifshitz J, Boockvar J, Neugebauer E, Snyder EY, McIntosh TK. Transplanted neural stem cells survive, differentiate, and improve neurological motor function after experimental traumatic brain injury. Neurosurgery. 2002 Oct;51(4):1043-52; discussion 1052-4. [CrossRef] [PubMed]

15. Philips MF, Mattiasson G, Wieloch T, Björklund A, Johansson BB, Tomasevic G, Martínez-Serrano A, Lenzlinger PM, Sinson G, Grady MS, McIntosh TK. Neuroprotective and behavioral efficacy of nerve growth factor-transfected hippocampal progenitor cell transplants after experimental traumatic brain injury. J Neurosurg. 2001 May;94(5):765-74. [CrossRef] [PubMed]

16. Haus DL, López-Velázquez L, Gold EM, Cunningham KM, Perez H, Anderson AJ, Cummings BJ. Transplantation of human neural stem cells restores cognition in an immunodeficient rodent model of traumatic brain injury. Exp Neurol. 2016 Jul;281:1-16. [CrossRef] [PubMed]

17. Elias PZ, Spector M. Implantation of a collagen scaffold seeded with adult rat hippocampal progenitors in a rat model of penetrating brain injury. J Neurosci Methods. 2012 Jul;209(1):199-211. [CrossRef] [PubMed]

18. Hagan M, Wennersten A, Meijer X, Holmin S, Wahlberg L, Mathiesen T. Neuroprotection by human neural progenitor cells after experimental contusion in rats. Neurosci Lett. 2003 Nov 20;351(3):149-52. [CrossRef] [PubMed]

19. Skardelly M, Gaber K, Burdack S, Scheidt F, Hilbig H, Boltze J, Förschler A, Schwarz S, Schwarz J, Meixensberger J, Schuhmann MU. Long-term benefit of human fetal neuronal progenitor cell transplantation in a clinically adapted model after traumatic brain injury. J Neurotrauma. 2011 Mar;28(3):401-14. [CrossRef] [PubMed]

20. Wallenquist U, Brännvall K, Clausen F, Lewén A, Hillered L, Forsberg-Nilsson K. Grafted neural progenitors migrate and form neurons after experimental traumatic brain injury. Restor Neurol Neurosci. 2009;27(4):323-34. [CrossRef] [PubMed]

21. Wennersten A, Meier X, Holmin S, Wahlberg L, Mathiesen T. Proliferation, migration, and differentiation of human neural stem/progenitor cells after transplantation into a rat model of traumatic brain injury. J Neurosurg. 2004 Jan;100(1):88-96. [CrossRef] [PubMed]

22. Zhang C, Saatman KE, Royo NC, Soltesz KM, Millard M, Schouten JW, Motta M, Hoover RC, McMillan A, Watson DJ, Lee VM, Trojanowski JQ, McIntosh TK. Delayed transplantation of human neurons following brain injury in rats: a long-term graft survival and behavior study. J Neurotrauma. 2005 Dec;22(12):1456-74. [CrossRef] [PubMed]

23. Harting MT, Sloan LE, Jimenez F, Baumgartner J, Cox CS Jr. Subacute neural stem cell therapy for traumatic brain injury. J Surg Res. 2009 May 15;153(2):188-94. [CrossRef] [PubMed] [PubMed Central]

24. Ma H, Yu B, Kong L, Zhang Y, Shi Y. Transplantation of neural stem cells enhances expression of synaptic protein and promotes functional recovery in a rat model of traumatic brain injury. Mol Med Rep. 2011 Sep-Oct;4(5):849-56. [CrossRef] [PubMed]

25. Dunkerson J, Moritz KE, Young J, Pionk T, Fink K, Rossignol J, Dunbar G, Smith JS. Combining enriched environment and induced pluripotent stem cell therapy results in improved cognitive and motor function following traumatic brain injury. Restor Neurol Neurosci. 2014;32(5):675-87. [CrossRef] [PubMed]

26. Wennersten A, Holmin S, Al Nimer F, Meijer X, Wahlberg LU, Mathiesen T. Sustained survival of xenografted human neural stem/progenitor cells in experimental brain trauma despite discontinuation of immunosuppression. Exp Neurol. 2006 Jun;199(2):339-47. [CrossRef] [PubMed]

27. Bakshi A, Shimizu S, Keck CA, Cho S, LeBold DG, Morales D, Arenas E, Snyder EY, Watson DJ, McIntosh TK. Neural progenitor cells engineered to secrete GDNF show enhanced survival, neuronal differentiation and improve cognitive function following traumatic brain injury. Eur J Neurosci. 2006 Apr;23(8):2119-34. [CrossRef] [PubMed]

28. Trojanowski JQ, Kleppner SR, Hartley RS, Miyazono M, Fraser NW, Kesari S, Lee VM. Transfectable and transplantable postmitotic human neurons: a potential «platform» for gene therapy of nervous system diseases. Exp Neurol. 1997 Mar;144(1):92-7. [CrossRef] [PubMed]

29. Tate CC, Shear DA, Tate MC, Archer DR, Stein DG, LaPlaca MC. Laminin and fibronectin scaffolds enhance neural stem cell transplantation into the injured brain. J Tissue Eng Regen Med. 2009 Mar;3(3):208-17. [CrossRef] [PubMed]

30. Ikeda R, Kurokawa MS, Chiba S, Yoshikawa H, Ide M, Tadokoro M, Nito S, Nakatsuji N, Kondoh Y, Nagata K, Hashimoto T, Suzuki N. Transplantation of neural cells derived from retinoic acid-treated cynomolgus monkey embryonic stem cells successfully improved motor function of hemiplegic mice with experimental brain injury. Neurobiol Dis. 2005 Oct;20(1):38-48. [CrossRef] [PubMed]

31. Chiba S, Iwasaki Y, Sekino H, Suzuki N. Transplantation of motoneuron-enriched neural cells derived from mouse embryonic stem cells improves motor function of hemiplegic mice. Cell Transplant. 2003;12(5):457-68. [CrossRef] [PubMed]

32. Chiba S, Ikeda R, Kurokawa MS, Yoshikawa H, Takeno M, Nagafuchi H, Tadokoro M, Sekino H, Hashimoto T, Suzuki N. Anatomical and functional recovery by embryonic stem cell-derived neural tissue of a mouse model of brain damage. J Neurol Sci. 2004 Apr 15;219(1-2):107-17. [CrossRef] [PubMed]

33. Walker PA, Bedi SS, Shah SK, Jimenez F, Xue H, Hamilton JA, Smith P, Thomas CP, Mays RW, Pati S, Cox CS Jr. Intravenous multipotent adult progenitor cell therapy after traumatic brain injury: modulation of the resident microglia population. J Neuroinflammation. 2012 Sep 28;9:228. [CrossRef] [PubMed] [PubMed Central]

34. Mahmood A, Lu D, Wang L, Li Y, Lu M, Chopp M. Treatment of traumatic brain injury in female rats with intravenous administration of bone marrow stromal cells. Neurosurgery. 2001 Nov;49(5):1196-203; discussion 1203-4">. [PubMed]

35. Castro RF, Jackson KA, Goodell MA, Robertson CS, Liu H, Shine HD. Failure of bone marrow cells to transdifferentiate into neural cells in vivo. Science. 2002 Aug 23;297(5585):1299. [CrossRef] [PubMed]

36. Sanchez-Ramos J, Song S, Cardozo-Pelaez F, Hazzi C, Stedeford T, Willing A, Freeman TB, Saporta S, Janssen W, Patel N, Cooper DR, Sanberg PR. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol. 2000 Aug;164(2):247-56. [CrossRef] [PubMed]

37. Qu K, Ortoleva P. Understanding stem cell differentiation through self-organization theory. J Theor Biol. 2008 Feb 21;250(4):606-20. [CrossRef] [PubMed]

38. Walker PA, Shah SK, Harting MT, Cox CS Jr. Progenitor cell therapies for traumatic brain injury: barriers and opportunities in translation. Dis Model Mech. 2009 Jan-Feb;2(1-2):23-38. [CrossRef] [PubMed] [PubMed Central]

39. Galindo LT, Filippo TR, Semedo P, Ariza CB, Moreira CM, Camara NO, Porcionatto MA. Mesenchymal stem cell therapy modulates the inflammatory response in experimental traumatic brain injury. Neurol Res Int. 2011;2011:564089. [CrossRef] [PubMed] [PubMed Central]

40. Chen XH, Iwata A, Nonaka M, Browne KD, Smith DH. Neurogenesis and glial proliferation persist for at least one year in the subventricular zone following brain trauma in rats. J Neurotrauma. 2003 Jul;20(7):623-31. [CrossRef] [PubMed]

41. Hong SQ, Zhang HT, You J, Zhang MY, Cai YQ, Jiang XD, Xu RX. Comparison of transdifferentiated and untransdifferentiated human umbilical mesenchymal stem cells in rats after traumatic brain injury. Neurochem Res. 2011 Dec;36(12):2391-400. [CrossRef] [PubMed]

42. Liu Y, Yi XC, Guo G, Long QF, Wang XA, Zhong J, Liu WP, Fei Z, Wang DM, Liu J. Basic fibroblast growth factor increases the transplantation mediated therapeutic effect of bone mesenchymal stem cells following traumatic brain injury. Mol Med Rep. 2014 Jan;9(1):333-9. [CrossRef] [PubMed]

43. Wang S, Kan Q, Sun Y, Han R, Zhang G, Peng T, Jia Y. Caveolin-1 regulates neural differentiation of rat bone mesenchymal stem cells into neurons by modulating Notch signaling. Int J Dev Neurosci. 2013 Feb;31(1):30-5. [CrossRef] [PubMed]

44. Huang SH, Wang L, Chi F, Wu CH, Cao H, Zhang A, Jong A. Circulating brain microvascular endothelial cells (cBMECs) as potential biomarkers of the bloodbrain barrier disorders caused by microbial and non-microbial factors. PLoS One. 2013.8(4):e62164. [CrossRef] [PubMed Central]

45. Zhang R, Liu Y, Yan K, Chen L, Chen XR, Li P, Chen FF, Jiang XD. Anti-inflammatory and immunomodulatory mechanisms of mesenchymal stem cell transplantation in experimental traumatic brain injury. J Neuroinflammation. 2013 Aug 23;10:106. [CrossRef] [PubMed] [PubMed Central]

46. Guo XB, Deng X, Wei Y. Homing of Cultured Endothelial Progenitor Cells and Their Effect on Traumatic Brain Injury in Rat Model. Sci Rep. 2017 Jun 23;7(1):4164. [CrossRef] [PubMed] [PubMed Central]

47. Gennai S, Monsel A, Hao Q, Liu J, Gudapati V, Barbier EL, Lee JW. Cell-based therapy for traumatic brain injury. Br J Anaesth. 2015 Aug;115(2):203-12. [CrossRef] [PubMed] [PubMed Central]

48. Guan J, Zhu Z, Zhao RC, Xiao Z, Wu C, Han Q, Chen L, Tong W, Zhang J, Han Q, Gao J, Feng M, Bao X, Dai J, Wang R. Transplantation of human mesenchymal stem cells loaded on collagen scaffolds for the treatment of traumatic brain injury in rats. Biomaterials. 2013 Aug;34(24):5937-46. [CrossRef] [PubMed]

49. Mahmood A, Lu D, Chopp M. Intravenous administration of marrow stromal cells (MSCs) increases the expression of growth factors in rat brain after traumatic brain injury. J Neurotrauma. 2004 Jan;21(1):33-9. [CrossRef] [PubMed]

50. Walker PA, Aroom KR, Jimenez F, Shah SK, Harting MT, Gill BS, Cox CS Jr. Advances in progenitor cell therapy using scaffolding constructs for central nervous system injury. Stem Cell Rev Rep. 2009 Sep;5(3):283-300. [CrossRef] [PubMed] [PubMed Central]

51. Lu D, Mahmood A, Wang L, Li Y, Lu M, Chopp M. Adult bone marrow stromal cells administered intravenously to rats after traumatic brain injury migrate into brain and improve neurological outcome. Neuroreport. 2001 Mar 5;12(3):559-63. [CrossRef] [PubMed]

52. Mahmood A, Lu D, Lu M, Chopp M. Treatment of traumatic brain injury in adult rats with intravenous administration of human bone marrow stromal cells. Neurosurgery. 2003 Sep;53(3):697-702; discussion 702-3. [CrossRef] [PubMed]

53. Chang CP, Chio CC, Cheong CU, Chao CM, Cheng BC, Lin MT. Hypoxic preconditioning enhances the therapeutic potential of the secretome from cultured human mesenchymal stem cells in experimental traumatic brain injury. Clin Sci (Lond). 2013 Feb;124(3):165-76. [CrossRef] [PubMed]

54. Barteneva NS, Maltsev N, Vorobjev IA. Microvesicles and intercellular communication in the context of parasitism. Front Cell Infect Microbiol. 2013 Sep 6;3:49. [CrossRef] [PubMed] [PubMed Central]

55. Escudero CA, Herlitz K, Troncoso F, Acurio J, Aguayo C, Roberts JM, Truong G, Duncombe G, Rice G, Salomon C. Role of Extracellular Vesicles and microRNAs on Dysfunctional Angiogenesis during Preeclamptic Pregnancies. Front Physiol. 2016 Mar 18;7:98. [CrossRef] [PubMed] [PubMed Central]

56. Zhang Y, Chopp M, Meng Y, Katakowski M, Xin H, Mahmood A, Xiong Y. Effect of exosomes derived from multipluripotent mesenchymal stromal cells on functional recovery and neurovascular plasticity in rats after traumatic brain injury. J Neurosurg. 2015 Apr;122(4):856-67. [CrossRef] [PubMed] [PubMed Central]

57. Mahmood A, Lu D, Chopp M. Marrow stromal cell transplantation after traumatic brain injury promotes cellular proliferation within the brain. Neurosurgery. 2004 Nov;55(5):1185-93. [CrossRef] [PubMed]

58. Park BN, Shim W, Lee G, Bang OY, An YS, Yoon JK, Ahn YH. Early distribution of intravenously injected mesenchymal stem cells in rats with acute brain trauma evaluated by (99m)Tc-HMPAO labeling. Nucl Med Biol. 2011 Nov;38(8):1175-82. [CrossRef] [PubMed]

59. Li L, Jiang Q, Qu CS, Ding GL, Li QJ, Wang SY, Lee JH, Lu M, Mahmood A, Chopp M. Transplantation of marrow stromal cells restores cerebral blood flow and reduces cerebral atrophy in rats with traumatic brain injury: in vivo MRI study. J Neurotrauma. 2011 Apr;28(4):535-45. [CrossRef] [PubMed] [PubMed Central]

60. Zanier ER, Montinaro M, Vigano M, Villa P, Fumagalli S, Pischiutta F, Longhi L, Leoni ML, Rebulla P, Stocchetti N, Lazzari L, De Simoni MG. Human umbilical cord blood mesenchymal stem cells protect mice brain after trauma. Crit Care Med. 2011 Nov;39(11):2501-10. [CrossRef] [PubMed]

61. Wang Z, Yao W, Deng Q, Zhang X, Zhang J. Protective effects of BDNF overexpression bone marrow stromal cell transplantation in rat models of traumatic brain injury. J Mol Neurosci. 2013 Feb;49(2):409-16. [CrossRef] [PubMed]

62. Bedi SS, Hetz R, Thomas C, Smith P, Olsen AB, Williams S, Xue H, Aroom K, Uray K, Hamilton J, Mays RW, Cox CS Jr. Intravenous multipotent adult progenitor cell therapy attenuates activated microglial/macrophage response and improves spatial learning after traumatic brain injury. Stem Cells Transl Med. 2013 Dec;2(12):953-60. [CrossRef] [PubMed] [PubMed Central]

63. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop Dj, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315-7. [CrossRef] [PubMed]

64. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature. 2002 Jul 4;418(6893):41-9. [CrossRef] [PubMed]

65. Walker PA, Shah SK, Jimenez F, Gerber MH, Xue H, Cutrone R, Hamilton JA, Mays RW, Deans R, Pati S, Dash PK, Cox CS Jr. Intravenous multipotent adult progenitor cell therapy for traumatic brain injury: preserving the blood brain barrier via an interaction with splenocytes. Exp Neurol. 2010 Oct;225(2):341-52. [CrossRef] [PubMed] [PubMed Central]

66. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006 Aug 25;126(4):663-76. [CrossRef] [PubMed]

67. Kobayashi Y, Okada Y, Itakura G, Iwai H, Nishimura S, Yasuda A, Nori S, Hikishima K, Konomi T, Fujiyoshi K, Tsuji O, Toyama Y, Yamanaka S, Nakamura M, Okano H. Pre-evaluated safe human iPSC-derived neural stem cells promote functional recovery after spinal cord injury in common marmoset without tumorigenicity. PLoS One. 2012;7(12):e52787. [CrossRef] [PubMed] [PubMed Central]

68. Gao X, Wang X, Xiong W, Chen J. In vivo reprogramming reactive glia into iPSCs to produce new neurons in the cortex following traumatic brain injury. Sci Rep. 2016 Mar 9;6:22490. [CrossRef] [PubMed] [PubMed Central]

69. Lyu Q, Zhang ZB, Fu SJ, Xiong LL, Liu J, Wang TH. Microarray Expression Profile of lncRNAs and mRNAs in Rats with Traumatic Brain Injury after A2B5+ Cell Transplantation. Cell Transplant. 2017 Oct;26(10):1622-1635. [CrossRef] [PubMed] [PubMed Central]

70. Dekmak A, Mantash S, Shaito A, Toutonji A, Ramadan N, Ghazale H, Kassem N, Darwish H, Zibara K. Stem cells and combination therapy for the treatment of traumatic brain injury. Behav Brain Res. 2018 Mar 15;340:49-62. [CrossRef] [PubMed]

71. Spees JL, Olson SD, Ylostalo J, Lynch PJ, Smith J, Perry A, Peister A, Wang MY, Prockop DJ. Differentiation, cell fusion, and nuclear fusion during ex vivo repair of epithelium by human adult stem cells from bone marrow stroma. Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2397-402. [CrossRef] [PubMed] [PubMed Central]

72. Tajiri N, Kaneko Y, Shinozuka K, Ishikawa H, Yankee E, McGrogan M, Case C, Borlongan CV. Stem cell recruitment of newly formed host cells via a successful seduction? Filling the gap between neurogenic niche and injured brain site. PLoS One. 2013 Sep 4;8(9):e74857. [CrossRef] [PubMed] [PubMed Central]

73. Alvarez-Buylla A, Garcia-Verdugo JM. Neurogenesis in adult subventricular zone. J Neurosci. 2002 Feb 1;22(3):629-34. [CrossRef] [PubMed] [PubMed Central]

74. Gonzalez-Perez O, Romero-Rodriguez R, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A. Epidermal growth factor induces the progeny of subventricular zone type B cells to migrate and differentiate into oligodendrocytes. Stem Cells. 2009 Aug;27(8):2032-43. [CrossRef] [PubMed] [PubMed Central]

75. Liu XS, Zhang ZG, Zhang RL, Gregg SR, Wang L, Yier T, Chopp M. Chemokine ligand 2 (CCL2) induces migration and differentiation of subventricular zone cells after stroke. J Neurosci Res. 2007 Aug 1;85(10):2120-5. [CrossRef] [PubMed]

76. Lois C, Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):2074-7. [CrossRef] [PubMed] [PubMed Central]

77. Seri B, García-Verdugo JM, McEwen BS, Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci. 2001 Sep 15;21(18):7153-60. [CrossRef] [PubMed] [PubMed Central]

78. Seri B, García-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol. 2004 Oct 25;478(4):359-78. [CrossRef] [PubMed]

79. So K, Moriya T, Nishitani S, Takahashi H, Shinohara K. The olfactory conditioning in the early postnatal period stimulated neural stem/progenitor cells in the subventricular zone and increased neurogenesis in the olfactory bulb of rats. Neuroscience. 2008 Jan 2;151(1):120-8. [CrossRef] [PubMed]


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