Intravenous transplants of human adipose-derived stem cell protect the brain from traumatic brain injury-induced neurodegeneration and motor and cognitive impairments: Cell graft biodistribution and soluble factors in young and aged rats

Journal of Neuroscience

Volumn 34, Issue 1, 2014, Pages 313-326

  Tajiri, Naoki ^a   Acosta, Sandra A ^a   Shahaduzzaman, Md ^a,b   Ishikawa, Hiroto ^a   Shinozuka, Kazutaka ^a   Pabon, Mibel ^a   Hernandez Ontiveros, Diana ^a   Kim, Dae Won ^a   Metcalf, Christopher ^a   Staples, Meaghan ^a   Dailey, Travis ^a   Vasconcellos, Julie ^a   Franyuti, Giorgio ^a   Gould, Lisa ^a,b   Patel, Niketa ^a,b   Cooper, Denise ^a,b   Kaneko, Yuji ^a   Borlongan, Cesar V ^a   Bickford, Paula C ^a,b  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Aging; Brain injury; Stem cell

Indexed keywords

ADIPOSE DERIVED STEM CELL; AKINESIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CELL TRANSPLANTATION; CELLULAR DISTRIBUTION; COGNITIVE DEFECT; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MALE; MORRIS WATER MAZE TEST; MOTOR DYSFUNCTION; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL LEARNING; TASK PERFORMANCE; TRAUMATIC BRAIN INJURY;

EID: 84891455213     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2425-13.2014     Document Type: Article

References (69)

1. Acosta SA, Tajiri N, Shinozuka K, Ishikawa H, Grimmig B, Diamond D, Sanberg PR, Bickford PC, Kaneko Y, Borlongan CV (2013) Long-term upregulation of inflammation and suppression of cell proliferation in the brain of adult rats exposed to traumatic brain injury using the controlled cortical impact model. PLoS One 8:e53376. CrossRef Medline
2. Ajmo CT Jr, Vernon DO, Collier L, Hall AA, Garbuzova-Davis S, Willing A, Pennypacker KR (2008) The spleen contributes to stroke-induced neurodegeneration. J Neurosci Res 86:2227-2234. CrossRef Medline
3. Arslan F, Lai RC, Smeets MB, Akeroyd L, Choo A, Aguor EN, Timmers L, van Rijen HV, Doevendans PA, Pasterkamp G, Lim SK, de Kleijn DP (2013) Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Res 10:301-312. CrossRef Medline
4. Baek SJ, Kang SK, Ra JC (2011) In vitro migration capacity of human adipose tissue-derived mesenchymal stem cells reflects their expression of receptors for chemokines and growth factors. Exp Mol Med 43:596-603. CrossRef Medline
5. Bernard D, Prasanth KV, Tripathi V, Colasse S, Nakamura T, Xuan Z, Zhang MQ, Sedel F, Jourdren L, Coulpier F, Triller A, Spector DL, Bessis A (2010) A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expression. EMBO J 29:3082-3093. CrossRef Medline
6. Bjorklund LM, Sánchez-Pernaute R, Chung S, Andersson T, Chen IY, Mc-Naught KS, Brownell AL, Jenkins BG, Wahlestedt C, Kim KS, Isacson O (2002) Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc Natl Acad Sci U S A 99:2344-2349. CrossRef Medline
7. Bjugstad KB, Teng YD, RedmondDEJr, Elsworth JD, Roth RH, Cornelius SK, Snyder EY, Sladek JR Jr (2008) Human neural stem cells migrate along the nigrostriatal pathway in a primate model of Parkinson's disease. Exp Neurol 211:362-369. CrossRef Medline
8. Blaber SP, Webster RA, Hill CJ, Breen EJ, Kuah D, Vesey G, Herbert BR (2012) Analysis of in vitro secretion profiles from adipose-derived cell populations. J Transl Med 10:172. CrossRef Medline
9. Boddington S, Henning TD, Sutton EJ, Daldrup-Link HE (2008) Labeling stem cells with fluorescent dyes for non-invasive detection with optical imaging. J Vis Exp (14):pii:686. CrossRef
10. Bond CS, Fox AH (2009) Paraspeckles: nuclear bodies built on long noncoding RNA. J Cell Biol 186:637-644. CrossRef Medline
11. Borlongan CV, Sanberg PR (1995) Elevated body swing test: a new behavioral parameter for rats with 6-hydroxydopamine-induced hemiparkinsonism. J Neurosci 15:5372-5378. Medline
12. Borlongan CV, Hida H, Nishino H (1998) Early assessment of motor dysfunctions aids in successful occlusion of the middle cerebral artery. Neuroreport 9:3615-3621. CrossRef Medline
13. Carlson ME, Conboy IM (2007) Loss of stem cell regenerative capacity within aged niches. Aging Cell 6:371-382. CrossRef Medline
14. Cho YJ, Song HS, Bhang S, Lee S, Kang BG, Lee JC, An J, Cha CI, Nam DH, Kim BS, JooKM (2012) Therapeutic effects of human adipose stem cellconditioned medium on stroke. J Neurosci Res 90:1794-1802. CrossRef Medline
15. Clarkson ED (2001) Fetal tissue transplantation for patients with Parkinson's disease: a database of published clinical results. Drugs Aging 18:773-785. CrossRef Medline
16. Clemson CM, Hutchinson JN, Sara SA, Ensminger AW, Fox AH, Chess A, Lawrence JB (2009) An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol Cell 33: 717-726. CrossRef Medline
17. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA (2005) Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433:760-764. CrossRef Medline
18. Darkazalli A, Levenson CW (2012) Tracking stem cell migration and survival in brain injury: current approaches and future prospects. Histol Histopathol 27:1255-1261. Medline
19. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown JB, Lipovich L, Gonzalez JM, Thomas M, Davis CA, Shiekhattar R, Gingeras TR, Hubbard TJ, Notredame C, Harrow J, Guigó R (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22:1775-1789. CrossRef Medline
20. Detante O, Moisan A, Dimastromatteo J, Richard MJ, Riou L, Grillon E, Barbier E, Desruet MD, De Fraipont F, Segebarth C, Jaillard A, Hommel M, Ghezzi C, Remy C (2009) Intravenous administration of 99mTc-HMPAO-labeled human mesenchymal stem cells after stroke: in vivo imaging and biodistribution. Cell Transplant 18:1369-1379. CrossRef Medline
21. Egashira Y, Sugitani S, Suzuki Y, Mishiro K, Tsuruma K, Shimazawa M, Yoshimura S, Iwama T, Hara H (2012) The conditioned medium of murine and human adipose-derived stem cells exerts neuroprotective effects against experimental stroke model. Brain Res 1461:87-95. CrossRef Medline
22. Faul M, Xu L, Wanld MM, Coronado VG (2010) Traumatic brain injury in the United States: emergency department visits, hospitalizations, and deaths. Atlanta GA: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control.
23. Fox AH, Lamond AI (2010) Paraspeckles. Cold Spring Harbor Perspect Biol 2:a000687.
24. Fraser JK, Wulur I, Alfonso Z, Hedrick MH (2006) Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol 24: 150-154. CrossRef Medline
25. Galindo LT, Filippo TR, Semedo P, Ariza CB, Moreira CM, Camara NO, Porcionatto MA (2011) Mesenchymal stem cell therapy modulates the inflammatory response in experimental traumatic brain injury. Neurol Res Int 2011:564089. Medline
26. Glover LE, Tajiri N, Lau T, Kaneko Y, van Loveren H, Borlongan CV (2012) Immediate, but not delayed, microsurgical skull reconstruction exacerbates brain damage in experimental traumatic brain injury model. PLoS One 7:e33646. CrossRef Medline
27. Harting MT, Sloan LE, Jimenez F, Baumgartner J, Cox CS Jr (2009) Subacute neural stem cell therapy for traumatic brain injury. J Surg Res 153: 188-194. CrossRef Medline
28. Hawkins BE, Cowart JC, Parsley MA, Capra BA, Eidson KA, Hellmich HL, Dewitt DS, Prough DS (2013) Effects of trauma, hemorrhage and resuscitation in aged rats. Brain Res 1496:28-35. CrossRef Medline
29. Hayashi T, Kaneko Y, Yu S, Bae E, Stahl CE, Kawase T, van Loveren H, Sanberg PR, Borlongan CV (2009) Quantitative analyses of matrix metalloproteinase activity after traumatic brain injury in adult rats. Brain Res 1280:172-177. CrossRef Medline
30. Ibrahim AG, Raisman G, Li Y (2009) Permanent loss of fore-paw grasping requires complete deprivation of afferent input from a minimum of four dorsal roots of the rat brachial plexus. Exp Neurol 215:142-145. CrossRef Medline
31. Ikegame Y, Yamashita K, Hayashi S, Mizuno H, Tawada M, You F, Yamada K, Tanaka Y, Egashira Y, Nakashima S, Yoshimura S, Iwama T (2011) Comparison of mesenchymal stem cells from adipose tissue and bone marrow for ischemic stroke therapy. Cytotherapy 13:675-685. CrossRef Medline
32. Isacson O, Costantini L, Schumacher JM, Cicchetti F, Chung S, Kim K (2001) Cell implantation therapies for Parkinson's disease using neural stem, transgenic or xenogeneic donor cells. Parkinsonism Relat Disord 7:205-212. CrossRef Medline
33. Jang YY, Ye Z, Cheng L (2011) Molecular imaging and stem cell research. Mol Imaging 10:111-122. Medline
34. Katsuda T, Tsuchiya R, Kosaka N, Yoshioka Y, Takagaki K, Oki K, Takeshita F, Sakai Y, Kuroda M, Ochiya T (2013) Human adipose tissue-derived mesenchymal stem cells secrete functional neprilysin-bound exosomes. Sci Rep 3:1197. CrossRef Medline
35. Kim WS, Park BS, Sung JH, Yang JM, Park SB, Kwak SJ, Park JS (2007) Wound healing effect of adipose-derived stem cells: a critical role of secretory factors on human dermal fibroblasts. J Dermatol Sci 48:15-24. CrossRef Medline
36. Lee P, Kim J, Williams R, Sandhir R, Gregory E, Brooks WM, Berman NE (2012) Effects of aging on blood brain barrier and matrix metalloproteases following controlled cortical impact in mice. Exp Neurol 234:50-61. CrossRef Medline
37. Lefebvre JS, Maue AC, Eaton SM, Lanthier PA, Tighe M, Haynes L (2012) The aged microenvironment contributes to the age-related functional defects of CD4 T cells in mice. Aging Cell 11:732-740. CrossRef Medline
38. Lendeckel S, Jödicke A, Christophis P, Heidinger K, Wolff J, Fraser JK, Hedrick MH, Berthold L, Howaldt HP (2004) Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report. J Craniomaxillofac Surg 32:370-373. CrossRef Medline
39. Li M, Li F, Luo C, Shan Y, Zhang L, Qian Z, Zhu G, Lin J, Feng H (2011) Immediate splenectomy decreases mortality and improves cognitive function of rats after severe traumatic brain injury. J Trauma 71:141-147. CrossRef Medline
40. Lindvall O, Brundin P, Widner H, Rehncrona S, Gustavii B, Frackowiak R, Leenders KL, Sawle G, Rothwell JC, Marsden CD, Bjorkland A (1990) Grafts of fetal dopamine neurons survive and improve motor function in Parkinson's disease. Science 247:574-577. CrossRef Medline
41. Liu YP, Lang BT, Baskaya MK, Dempsey RJ, Vemuganti R (2009) The potential of neural stem cells to repair stroke-induced brain damage. Acta Neuropathol 117:469-480. CrossRef Medline
42. Mahmood A, Lu D, Lu M, Chopp M (2003) Treatment of traumatic brain injury in adult rats with intravenous administration of human bone marrow stromal cells. Neurosurgery 53:697-702; discussion 702-703. CrossRef Medline
43. McDonald KG, Leach MR, Huang C, Wang C, Newberry RD (2011) Aging impacts isolated lymphoid follicle development and function. Immunity Ageing 8:1. CrossRef Medline
44. Mercer TR, Mattick JS (2013) Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol 20:300-307. CrossRef Medline
45. Michalet X, Pinaud FF, Bentolila LA, Tsay JM, Doose S, Li JJ, Sundaresan G, Wu AM, Gambhir SS, Weiss S (2005) Quantum dots for live cells, in vivo imaging, and diagnostics. Science 307:538-544. CrossRef Medline
46. Mizuno H, Tobita M, Uysal AC (2012) Concise review: adipose-derived stem cells as a novel tool for future regenerative medicine. Stem Cells 30:804-810. CrossRef Medline
47. Muraoka K, Shingo T, Yasuhara T, Kameda M, Yuen WJ, Uozumi T, Matsui T, Miyoshi Y, Date I (2008) Comparison of the therapeutic potential of adult and embryonic neural precursor cells in a rat model of Parkinson disease. J Neurosurg 108:149-159. CrossRef Medline
48. Naganuma T, Hirose T (2013) Paraspeckle formation during the biogenesis of long non-coding RNAs. RNA Biol 10(8). CrossRef
49. Nakagawa S, Hirose T (2012) Paraspeckle nuclear bodies-useful uselessness? Cell Mol Life Sci 69:3027-3036. CrossRef Medline
50. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, Ed 6. Amsterdam: Academic/Elsevier.
51. Qi JH, Ebrahem Q, Moore N, Murphy G, Claesson-Welsh L, Bond M, Baker A, Anand-Apte B (2003) A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2. Nat Med 9:407-415. CrossRef Medline
52. Ribeiro CA, Fraga JS, Grãos M, Neves NM, Reis RL, Gimble JM, Sousa N, Salgado AJ (2012) The secretome of stem cells isolated from the adipose tissue and Wharton jelly acts differently on central nervous system derived cell populations. Stem Cell Res Ther 3:18. CrossRef Medline
53. Sasaki YT, Ideue T, Sano M, Mituyama T, Hirose T (2009) MENepsilon/ beta noncoding RNAs are essential for structural integrity of nuclear paraspeckles. Proc Natl Acad Sci U S A 106:2525-2530. CrossRef Medline
54. Singer NG, Caplan AI (2011) Mesenchymal stem cells: mechanisms of inflammation. Annu Rev Pathol 6:457-478. CrossRef Medline
55. SolantoMV (1984) Neuropharmacological basis of stimulant drug action in attention deficit disorder with hyperactivity: a review and synthesis. Psychol Bull 95:387-409. CrossRef Medline
56. Spadaro PA, Bredy TW (2012) Emerging role of non-coding RNA in neural plasticity, cognitive function, and neuropsychiatric disorders. Front Genet 3:132. CrossRef Medline
57. Sugiyama T, Kuroda S, Osanai T, Shichinohe H, Kuge Y, Ito M, Kawabori M, Iwasaki Y (2011) Near-infrared fluorescence labeling allows noninvasive tracking of bone marrow stromal cells transplanted into rat infarct brain. Neurosurgery 68:1036-1047; discussion 1047. CrossRef Medline
58. Sun J, Zhou H, Deng Y, Zhang Y, Gu P, Ge S, Fan X (2012) Conditioned medium from bone marrow mesenchymal stem cells transiently retards osteoblast differentiation by downregulating runx2. Cells Tissues Organs 196:510-522. CrossRef Medline
59. Ushiki T, Kizaka-Kondoh S, Ashihara E, Tanaka S, Masuko M, Hirai H, Kimura S, Aizawa Y, Maekawa T, HiraokaM (2010) Noninvasive tracking of donor cell homing by near-infrared fluorescence imaging shortly after bone marrow transplantation. PLoS One 5:e11114. CrossRef Medline
60. Vendrame M, Gemma C, Pennypacker KR, Bickford PC, Davis Sanberg C, Sanberg PR, Willing AE (2006) Cord blood rescues stroke-induced changes in splenocyte phenotype and function. Exp Neurol 199:191-200. CrossRef Medline
61. Vorhees CV, Williams MT (2006) Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1:848-858. CrossRef Medline
62. Walker PA, Shah SK, Harting MT, Cox CS Jr (2009) Progenitor cell therapies for traumatic brain injury: barriers and opportunities in translation. Dis Model Mech 2:23-38. CrossRef Medline
63. 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 (2010) Intravenous multipotent adult progenitor cell therapy for traumatic brain injury: preserving the blood brain barrier via an interaction with splenocytes. Exp Neurol 225:341-352. CrossRef Medline
64. Wapinski O, Chang HY (2011) Long noncoding RNAs and human disease. Trends Cell Biol 21:354-361. CrossRef Medline
65. Xue S, Zhang HT, Zhang P, Luo J, Chen ZZ, Jang XD, Xu RX (2010) Functional endothelial progenitor cells derived from adipose tissue show beneficial effect on cell therapy of traumatic brain injury. Neurosci Lett 473: 186-191. CrossRef Medline
66. Yang M, Donaldson AE, Jiang Y, Iacovitti L (2003) Factors influencing the differentiation of dopaminergic traits in transplanted neural stem cells. Cell Mol Neurobiol 23:851-864. CrossRef Medline
67. Yao J, Jiang SL, Liu W, Liu C, Chen W, Sun L, Liu KY, Jia ZB, Li RK, Tian H (2012) Tissue inhibitor of matrix metalloproteinase-3 or vascular endothelial growth factor transfection of aged human mesenchymal stem cells enhances cell therapy after myocardial infarction. Rejuvenation Res 15: 495-506. CrossRef Medline
68. Yu S, Kaneko Y, Bae E, Stahl CE, Wang Y, van Loveren H, Sanberg PR, Borlongan CV (2009) Severity of controlled cortical impact traumatic brain injury in rats and mice dictates degree of behavioral deficits. Brain Res 1287:157-163. CrossRef Medline
69. Zhang B, Arun G, Mao YS, Lazar Z, Hung G, Bhattacharjee G, Xiao X, Booth CJ, Wu J, Zhang C, Spector DL (2012) The lncRNA Malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult. Cell Rep 2:111-123. CrossRef Medline