Cell proliferation and neuroblast differentiation in the rat dentate gyrus after intrathecal treatment with adipose-derived mesenchymal stem cells

Cellular and Molecular Neurobiology

Volumn 31, Issue 8, 2011, Pages 1271-1280

  Choi, Jung Hoon ^a   Chung, Jin Young ^b,c   Yoo, Dae Young ^b   Hwang, In Koo ^b   Yoo, Ki Yeon ^d   Lee, Choong Hyun ^a   Yan, Bing Chun ^a   Ahn, Jin Ok ^b   Youn, Hwa Young ^b   Won, Moo Ho ^a  

^a Kangwon National University   (South Korea)

^b Seoul National University   (South Korea)

^c Seoul National University Hospital   (South Korea)

^d Gangneung Wonju National University   (South Korea)

Author keywords

Doublecortin; Hippocampus; Ki67; Neurogenesis; Subgranular zone

Indexed keywords

DOUBLECORTIN; KI 67 ANTIGEN; BIOLOGICAL MARKER;

ADIPOSE DERIVED MESENCHYMAL STEM CELL TRANSPLANATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CEREBELLUM; CISTERNA MAGNA; CONTROLLED STUDY; DENTATE GYRUS; DIENCEPHALON; HIPPOCAMPUS; IMMUNOCOMPETENT CELL; MALE; MEDULLA OBLONGATA; MENINX; MESENCEPHALON; MESENCHYMAL STEM CELL TRANSPLANTATION; NEUROBLAST; NONHUMAN; RAT; SPINAL CORD; WESTERN BLOTTING; ADIPOSE TISSUE; ANIMAL; CELL MOTION; CYTOLOGY; INTRASPINAL DRUG ADMINISTRATION; MESENCHYMAL STEM CELL; METABOLISM; METHODOLOGY; PHYSIOLOGY; WISTAR RAT;

ADIPOSE TISSUE; ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; DENTATE GYRUS; INJECTIONS, SPINAL; KI-67 ANTIGEN; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; RATS; RATS, WISTAR;

EID: 84860861637     PISSN: 02724340     EISSN: 15736830     Source Type: Journal    
DOI: 10.1007/s10571-011-9729-7     Document Type: Article

References (56)

1. Bain MJ, Dwyer SM, Rusak B (2004) Restraint stress affects hippocampal cell proliferation differently in rats and mice. Neurosci Lett 368:7-10
2. Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM (2001) Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 98:2396-2402
3. Canola K, Angenieux B, Tekaya M, Quiambao A, Naash MI, Munier FL, Schorderet DF, Arsenijevic Y (2007) Retinal stem cells transplanted into models of late stages of retinitis pigmentosa preferentially adopt a glial or a retinal ganglion cell fate. Invest Ophthalmol Vis Sci 48:446-454
4. Caterson EJ, Nesti LJ, Albert T, Danielson K, Tuan R (2001) Application of mesenchymal stem cells in the regeneration of musculoskeletal tissues. MedGenMed 3(1):E1
5. Cheng FJ, Zou P, Zhong ZD, Guo R, Xiao J (2003) The growth characteristics of mesenchymal stem/progenitor cells in human umbilical cord blood. Zhongguo Shi Yan Xue Ye Xue Za Zhi 11:565-568
6. Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, Bogdahn U, Winkler J, Kuhn HG, Aigner L (2005) Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21:1-14
7. Diederichsen AC, Møller JE, Thayssen P, Junker AB, Videbaek L, Saekmose SG, Barington T, Kristiansen M, Kassem M (2008) Effect of repeated intracoronary injection of bone marrow cells in patients with ischaemic heart failure the Danish stem cell study-congestive heart failure trial (DanCell-CHF). Eur J Heart Fail 10:661-667
8. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for cellular therapy position statement. Cytotherapy 8:315-317
9. Erices A, Conget P, Minguell JJ (2000) Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 109:235-242
10. Fortier LA, Travis AJ (2011) Stem cells in veterinary medicine. Stem Cell Res Ther 2:9
11. Gnecchi M, Zhang Z, Ni A, Dzau VJ (2008) Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 103:1204-1219
12. Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17:2492-2498
13. Guzman R, Bliss T, De Los Angeles A, Moseley M, Palmer T, Steinberg G (2008) Neural progenitor cells transplanted into the uninjured brain undergo targeted migration after stroke onset. J Neurosci Res 86:873-882
14. Habisch HJ, Janowski M, Binder D, Kuzma-Kozakiewicz M, Widmann A, Habich A, Schwalenstöcker B, Hermann A, Brenner R, Lukomska B, Domanska-Janik K, Ludolph AC, Storch A (2007) Intrathecal application of neuroectodermally converted stem cells into a mouse model of ALS: limited intraparenchymal migration and survival narrows therapeutic effects. J Neural Transm 114:1395-1406
15. Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A (2005) Clarification of the nomenclature for MSC: The International Society for cellular therapy position statement. Cytotherapy 7: 393-395
16. Hylden JL, Wilcox GL (1980) Intrathecal morphine in mice: a new technique. Eur J Pharmacol 67:313-316
17. Ito T, Suzuki A, Okabe M, Imai E, Hori M (2001) Application of bone marrow-derived stem cells in experimental nephrology. Exp Nephrol 9:444-450
18. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115:97-105
19. Kee N, Teixeira CM, Wang AH, Frankland PW (2007) Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 10:355-362
20. Kempermann G, Kuhn HG, Gage FH (1997) Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci USA 94:10409-10414
21. Kim H, Kim HY, Choi MR, Hwang S, Nam KH, Kim HC, Han JS, Kim KS, Yoon HS, Kim SH (2010) Dose-dependent efficacy of ALS-human mesenchymal stem cells transplantation into cisterna magna in SOD1-G93A ALS mice. Neurosci Lett 468:190-194
22. Kinnaird T, Stabile E, Burnett MS, Lee CW, Barr S, Fuchs S, Epstein SE (2004a) Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 94:678-685
23. Kinnaird T, Stabile E, Burnett MS, Shou M, Lee CW, Barr S, Fuchs S, Epstein SE (2004b) Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 109:1543-1549
24. Komatsu K, Honmou O, Suzuki J, Houkin K, Hamada H, Kocsis JD (2010) Therapeutic time window of mesenchymal stem cells derived from bone marrow after cerebral ischemia. Brain Res 1334:84-92
25. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033
26. Lagace DC, Donovan MH, DeCarolis NA, Farnbauch LA, Malhotra S, Berton O, Nestler EJ, Krishnan V, Eisch AJ (2010) Adult hippocampal neurogenesis is functionally important for stressinduced social avoidance. Proc Natl Acad Sci USA 107:4436-4441
27. Lee JH, Chung WH, Kang EH, Chung DJ, Choi CB, Chang HS, Hwang SH, Han H, Choe BY, Kim HY (2011) Schwann cell-like remyelination following transplantation of human umbilical cord blood (hUCB)-derived mesenchymal stem cells in dogs with acute spinal cord injury. J Neurol Sci 300:86-96
28. Lepore AC, Bakshi A, Swanger SA, Rao MS, Fischer I (2005) Neural precursor cells can be delivered into the injured cervical spinal cord by intrathecal injection at the lumbar cord. Brain Res 1045: 206-216
29. Liu W, Jiang X, Fu X, Cui S, Du M, Cai Y, Xu R (2008) Bone marrow stromal cells can be delivered to the site of traumatic brain injury via intrathecal transplantation in rabbits. Neurosci Lett 434:160-164
30. Liu Y, Liu T, Ma X, Fan X, Bao C, Cui Z (2009) Effects of encapsulated rabbit mesenchymal stem cells on ex vivo expansion of human umbilical cord blood hematopoietic stem/ progenitor cells. J Microencapsul 26:130-142
31. Madhavan L, Daley BF, Paumier KL, Collier TJ (2009) Transplantation of subventricular zone neural precursors induces an endogenous precursor cell response in a rat model of Parkinson's disease. J Comp Neurol 515:102-115
32. Mahmood A, Lu D, Chopp M (2004) Marrow stromal cell transplantation after traumatic brain injury promotes cellular proliferation within the brain. Neurosurgery 55:1185-1193
33. Minguell JJ, Florenzano FM, Ramírez MR, Martínez RF, Lasala GP (2010) Intracoronary infusion of a combination of bone marrowderived stem cells in dogs. Exp Clin Cardiol 15:17-20
34. Morita E, Watanabe Y, Ishimoto M, Nakano T, Kitayama M, Yasui K, Fukada Y, Doi K, Karunaratne A, Murrell WG, Sutharsan R, Mackay-Sim A, Hata Y, Nakashima K (2008) A novel cell transplantation protocol and its application to an ALS mouse model. Exp Neurol 213:431-438
35. Nacher J, Crespo C, McEwen BS (2001) Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 14:629-644
36. Nervi B, Link DC, DiPersio JF (2006) Cytokines and hematopoietic stem cell mobilization. J Cell Biochem 99:690-705
37. Neupane M, Chang CC, Kiupel M, Yuzbasiyan-Gurkan V (2008) Isolation and characterization of canine adipose-derived mesenchymal stem cells. Tissue Eng Part A 14:1007-1015
38. Newby AC (2006) Matrix metalloproteinases regulate migration, proliferation, and death of vascular smooth muscle cells by degrading matrix and non-matrix substrates. Cardiovasc Res 69:614-624
39. Pavlichenko N, Sokolova I, Vijde S, Shvedova E, Alexandrov G, Krouglyakov P, Fedotova O, Gilerovich EG, Polyntsev DG, Otellin VA (2008) Mesenchymal stem cells transplantation could be beneficial for treatment of experimental ischemic stroke in rats. Brain Res 1233:203-213
40. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates, 5th edn. Elsevier Academic Press, Amsterdam
41. Picard-Riera N, Nait-Oumesmar B, Baron-Van Evercooren A (2004) Endogenous adult neural stem cells: limits and potential to repair the injured central nervous system. J Neurosci Res 76:223-231
42. Poh KK, Sperry E, Young RG, Freyman T, Barringhaus KG, Thompson CA (2007) Repeated direct endomyocardial transplantation of allogeneic mesenchymal stem cells: safety of a high dose, "off-theshelf", cellular cardiomyoplasty strategy. Int J Cardiol 117:360-364
43. Prockop DJ (2007) "Stemness" does not explain the repair of many tissues by mesenchymal stem/multipotent stromal cells (MSCs). Clin Pharmacol Ther 82:241-243
44. Ramirez-Amaya V, Marrone DF, Gage FH, Worley PF, Barnes CA (2006) Integration of new neurons into functional neural networks. J Neurosci 26:12237-12241
45. Saito F, Nakatani T, Iwase M, Maeda Y, Hirakawa A, Murao Y, Suzuki Y, Onodera R, Fukushima M, Ide C (2008) Spinal cord injury treatment with intrathecal autologous bone marrow stromal cell transplantation: the first clinical trial case report. J Trauma 64:53-59
46. Scholzen T, Gerdes J (2000) The Ki-67 protein: from the known and the unknown. J Cell Physiol 182:311-322
47. Shear DA, Tate MC, Archer DR, Hoffman SW, Hulce VD, Laplaca MC, Stein DG (2004) Neural progenitor cell transplants promote long-term functional recovery after traumatic brain injury. Brain Res 1026:11-22
48. Sugaya K (2003) Neuroreplacement therapy and stem cell biology under disease conditions. Cell Mol Life Sci 60:1891-1902
49. Sun L, Lee J, Fine HA (2004) Neuronally expressed stem cell factor induces neural stem cell migration to areas of brain injury. J Clin Invest 113:1364-1374
50. Taiwo OB, Kovács KJ, Larson AA (2005) Chronic daily intrathecal injections of a large volume of fluid increase mast cells in the thalamus of mice. Brain Res 1056:76-84
51. Terada M, Kuzumaki N, Hareyama N, Imai S, Niikura K, Narita M, Yamazaki M, Suzuki T (2008) Suppression of enriched environment-induced neurogenesis in a rodent model of neuropathic pain. Neurosci Lett 440:314-318
52. van Velthoven CT, Kavelaars A, van Bel F, Heijnen CJ (2010) Repeated mesenchymal stem cell treatment after neonatal hypoxia-ischemia has distinct effects on formation and maturation of new neurons and oligodendrocytes leading to restoration of damage, corticospinal motor tract activity, and sensorimotor function. J Neurosci 30:9603-9611
53. Veena J, Srikumar BN, Raju TR, Shankaranarayana Rao BS (2009) Exposure to enriched environment restores the survival and differentiation of new born cells in the hippocampus and ameliorates depressive symptoms in chronically stressed rats. Neurosci Lett 455:178-182
54. Vieira NM, Brandalise V, Zucconi E, Secco M, Strauss BE, Zatz M (2010) Isolation, characterization, and differentiation potential of canine adipose-derived stem cells. Cell Transplant 19:279-289
55. Yang J, Wu H, Hu N, Gu X, Ding F (2009) Effects of bone marrow stromal cell-conditioned medium on primary cultures of peripheral nerve tissues and cells. Neurochem Res 34:1685-1694
56. Zhu S, Lu Y, Zhu J, Xu J, Huang H, Zhu M, Chen Y, Zhou Y, Fan X, Wang Z (2011) Effects of intrahepatic bone-derived mesenchymal stem cells autotransplantation on the diabetic beagle dogs. J Surg Res 168:213-223