Delayed post-treatment with bone marrow-derived mesenchymal stem cells is neurorestorative of striatal medium-spiny projection neurons and improves motor function after neonatal rat hypoxia-ischemia

Molecular and Cellular Neuroscience

Volumn 68, Issue , 2015, Pages 56-72

  Cameron, Stella H ^a   Alwakeel, Amr J ^a   Goddard, Liping ^a   Hobbs, Catherine E ^a   Gowing, Emma K ^a   Barnett, Elizabeth R ^a   Kohe, Sarah E ^a   Sizemore, Rachel J ^a   Oorschot, Dorothy E ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Adult mesenchymal stem cells; Cavalieri's method; DARPP positive striatal neurons; Dose effect; Forepaw motor skills; Stereology; Striatal medium spiny projection neurons; Striatal neurorestoration; Subcutaneous injection

Indexed keywords

BROXURIDINE; CALRETININ; PHOSPHOPROTEIN DARPP 32; LEUKOCYTE ANTIGEN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BRAIN WEIGHT; CELL TRANSPLANTATION; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; CORPUS STRIATUM; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; MOTOR PERFORMANCE; NERVE CELL; NEWBORN; NEWBORN HYPOXIA; NONHUMAN; PRIORITY JOURNAL; RAT; STRIATAL MEDIUM SPINY PROJECTION NEURON; SUBVENTRICULAR ZONE; THERAPY DELAY; TREATMENT RESPONSE; AGE; ANIMAL; BIOLOGICAL THERAPY; BODY WEIGHT; COMPLICATION; CYTOLOGY; DISEASE MODEL; HYPOXIA-ISCHEMIA, BRAIN; LATERAL BRAIN VENTRICLE; MESENCHYMAL STROMA CELL; METABOLISM; MOTOR SKILLS DISORDERS; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT; TIME FACTOR;

ANIMALIA; RATTUS;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD; BODY WEIGHT; CALBINDIN 2; CELL- AND TISSUE-BASED THERAPY; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINE AND CAMP-REGULATED PHOSPHOPROTEIN 32; HYPOXIA-ISCHEMIA, BRAIN; LATERAL VENTRICLES; MALE; MESENCHYMAL STROMAL CELLS; MOTOR SKILLS DISORDERS; NEUROGENESIS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 84927548996     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2015.03.019     Document Type: Article

References (84)

1. Alexander G.E., DeLong M.R., Strick P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 1986, 9:357-381.
2. Anderson K.D., Reiner A. Immunohistochemical localization of DARPP-32 in striatal projection neurons and striatal interneurons: implications for the localization of D1-like dopamine receptors on different types of striatal neurons. Brain Res. 1991, 568:235-243.
3. Anjos-Afonso F., Siapati E.K., Bonnet D. In vivo contribution of murine mesenchymal stem cells into multiple cell-types under minimal damage conditions. J. Cell Sci. 2004, 117:5655-5664.
4. Bae S.-H., Kong T.-H., Lee H.-S., Kim K.-S., Hong K.S., Chopp M., Kang M.-S., Moon J. Long-lasting paracrine effects of human cord blood cells on damaged neocortex in an animal model of cerebral palsy. Cell Transplant. 2012, 21:2497-2515.
5. Bedi K. Effects of Undernutrition on Brain Morphology: A Critical Review of Methods and Results. Current Topics in Research on Synapses 1984, vol. 2:93-163. Alan R. Liss, Inc., New York.
6. Borlongan C.V., Hadman M., Sanberg C.D., Sanberg P.R. Central nervous system entry of peripherally injected umbilical cord blood cells is not required for neuroprotection in stroke. Stroke 2004, 35:2385-2389.
7. Boyce R.W., Dorph-Petersen K.-A., Lyck L., Gundersen H.J.G. Design-based stereology: introduction to basic concepts and practical approaches for estimation of cell number. Toxicol. Pathol. 2010, 38:1011-1025.
8. Braendgaard H., Evans S.M., Howard C.V., Gundersen H.J.G. The total number of neurons in the human neocortex unbiasedly estimated using optical disectors. J. Microsc. 1990, 157:285-304.
9. Chen J., Li Y., Chopp M. Intracerebral transplantation of bone marrow with BDNF after MCAo in rat. Neuropharmacology 2000, 39:711-716.
10. Chen J., Li Y., Katakowski M., Chen X.G., Wang L., Lu D.Y., Lu M., Gautam S.C., Chopp M. Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J. Neurosci. Res. 2003, 73:778-786.
11. Chmielnicki E., Benraiss A., Economides A.N., Goldman S.A. Adenovirally expressed noggin and brain-derived neurotrophic factor cooperate to induce new medium spiny neurons from resident progenitor cells in the adult striatal ventricular zone. J. Neurosci. 2004, 24:2133-2142.
12. Cho S.-R., Benraiss A., Chmielnicki E., Samdani A., Economides A., Goldman S.A. Induction of neostriatal neurogenesis slows disease progression in a transgenic murine model of Huntington disease. J. Clin. Investig. 2007, 117:2899-2902.
13. Constantin G., Marconi S., Rossi B., Angiari S., Calderan L., et al. Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells 2009, 27:2624-2635.
14. Covey M.V., Oorschot D.E. Effect of hypothermic post-treatment on hypoxic-ischemic striatal injury, and normal striatal development, in neonatal rats: a stereological study. Pediatr. Res. 2007, 62:646-651.
15. Dailey T., Mosley Y., Pabon M., Acosta S., Tajiri N., van Loveren H., Kaneko Y., Borlongan C.V. Advancing critical care medicine with stem cell therapy and hypothermia for cerebral palsy. NeuroReport 2013, 24:1067-1071.
16. Decressac M., Prestoz L., Veran J., Cantereau A., Jaber M., Gaillard A. Neuropeptide Y stimulates proliferation, migration and differentiation of neural precursors from the subventricular zone in adult mice. Neurobiol. Dis. 2009, 34:441-449.
17. Djouad F., Plence P., Bony C., Tropel P., Apparailly F., Sany J., Noel D., Jorgensen C. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 2003, 102:3837-3844.
18. Donega V., van Velthoven C.T.J., Nijboer C.H., Kavelaars A., Heijnen C.J. The endogenous regenerative capacity of the damaged newborn brain: boosting neurogenesis with mesenchymal stem cell treatment. J. Cereb. Blood Flow Metab. 2013, 33:625-634.
19. Felling R.J., Snyder M.J., Romanko M.J., Rothstein R.P., Ziegler A.N., Yang Z., Givogri M.I., Bongarzone E.R., Levison S.W. Neural stem/progenitor cells participate in the regenerative response to perinatal hypoxia/ischemia. J. Neurosci. 2006, 26:4359-4369.
20. Frenette P.S., Pinho S., Lucas D., Scheiermann C. Mesenchymal stem cell: keystone of the hematopoietic stem cell niche and a stepping-stone for regenerative medicine. Annu. Rev. Immunol. 2013, 31:285-316.
21. Galvin K.A., Oorschot D.E. Postinjury magnesium sulfate treatment is not markedly neuroprotective for striatal medium spiny neurons after perinatal hypoxia/ischemia in the rat. Pediatr. Res. 1998, 44:740-745.
22. Gao J., Dennis J.E., Muzic R.F., Lundberg M., Caplan A.I. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cell Tissue Organ 2001, 169:12-20.
23. Gerfen C.R., Staines W.A., Arbuthnott G.W., Fibiger H.C. Crossed connections of the substantia nigra in the rat. J. Comp. Neurol. 1982, 207:283-303.
24. Gordon D., Pavlovska G., Glover C.P., Uney J.B., Wraith D., Scolding N.J. Human mesenchymal stem cells abrogate experimental allergic encephalomyelitis after intraperitoneal injection, and with sparse CNS infiltration. Neurosci. Lett. 2008, 448:71-73.
25. Grabowski M., Brundin P., Johansson B.B. Paw-reaching, sensorimotor, and rotational behavior after brain infarction in rats. Stroke 1993, 24:889-895.
26. Grow J.L., Liu Y.Q., Barks J.D. Can lateralizing sensorimotor deficits be identified after neonatal cerebral hypoxia-ischemia in rats?. Dev. Neurosci. 2003, 25:394-402.
27. Gundersen H.J.G. Notes on the estimation of numerical density of arbitrary profiles: the edge effect. J. Microsc. 1977, 111:219-223.
28. Gundersen H.J.G., Jensen E.B.V., Kieu K., Nielsen J. The efficiency of systematic sampling in stereology - reconsidered. J. Microsc. 1999, 193:199-211.
29. Hess D.C., Borlongan C.V. Stem cells and neurological diseases. Cell Prolif. 2008, 41(Suppl. 1):94-114.
30. Hewlitt K.A., Corbett D. Delayed minocycline treatment reduces long-term functional deficits and histological injury in a rodent model of focal ischemia. Neurosciences 2006, 141:27-33.
31. Hill A. Current concepts of hypoxic-ischemic cerebral injury in the term newborn. Pediatr. Neurol. 1991, 7:317-325.
32. Hobbs C.E., Oorschot D.E. Neonatal rat hypoxia-ischemia: long-term rescue of striatal neurons and motor skills by combined antioxidant-hypothermia treatment. Brain Pathol. 2008, 18:443-454.
33. Im S.H., Yu J.H., Park E.S., Lee J.E., Kim H.O., Park K.I., Wim G.W., Park C.I., Cho S.-R. Induction of striatal neurogenesis enhances functional recovery in an adult animal model of neonatal hypoxic-ischemic brain injury. Neurosci. 2010, 169:259-268.
34. Larsen M., Bjarkam C.R., Ostergaard K., West M.J., Sørensen J.C. The anatomy of the porcine subthalamic nucleus evaluated with immunohistochemistry and design-based stereology. Anat. Embryol. 2004, 208:239-247.
35. Le Blanc K., Frassoni F., Ball L., Locatelli F., Roelofs H., Lewis I., Lanino E., Sundberg B., Bernado M.E., Remberger M., Dini G., Egeler R.M., Bacigalupo A., Fibbe W., Ringden O. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 2008, 371:1579-1586.
36. Lee J.A., Kim B.I., Jo C.H., Choi C.W., Kim E.-K., Kim H.-S., Yoon K.-S., Choi J.-H. Mesenchymal stem-cell transplantation for hypoxic-ischemic brain injury in neonatal rat model. Pediatr. Res. 2010, 67:42-46.
37. Li Y., Chopp M., Chen J., Wang L., Gautam S.C., Xu Y.-X., Zhang Z. Intrastriatal transplantation of bone marrow nonhematopoietic cells improves functional recovery after stroke in adult mice. J. Cereb. Blood Flow Metab. 2000, 20:1311-1319.
38. Liu Z., Li Y., Zhang Z.G., Cui X., Cui Y., Lu M., Savant-Bhonsale S., Chopp M. Bone marrow stromal cells enhance inter- and intracortical axonal connections after ischemic stroke in adult rats. J. Cereb. Blood Flow Metab. 2010, 30:1288-1295.
39. Luskin M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 1993, 11:173-189.
40. Montoya C.P., Campbell-Hope L.J., Pemberton K.D., Dunnett S.B. The "staircase test": a measure of independent forelimb reaching and grasping abilities in rats. J. Neurosci. Methods 1991, 36:219-228.
41. Moore N., Okocha F., Cui J.K., Liu P.K. Homogeneous repair of nuclear genes after experimental stroke. J. Neurochem. 2002, 80:111-118.
42. Nagaya N., Fujii T., Iwase T., Ohgushi H., Itoh T., Uematsu M., Yamagishi M., Mori H., Kangawa K., Kitamura S. Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis. Am. J. Physiol. Heart Circ. Physiol. 2004, 287:H2670-H2676.
43. Oh J.Y., Kim T.W., Jeong H.Y., Lee H.J., Ryu J.S., Wee W.R., Heo J.W., Kim M.K. Intraperitoneal infusion of mesenchymal stem/stromal cells prevents experimental autoimmune uveitis in mice. Mediators Inflamm. 2014, 10.1155/2014/624640.
44. Ong J., Plane J.M., Parent J.M., Silverstein F.S. Hypoxic-ischemic injury stimulates subventricular zone proliferation and neurogenesis in the neonatal rat. Pediatr. Res. 2005, 58:600-606.
45. Oorschot D.E. Are you using neuronal densities, synaptic densities or neurochemical densities as your definitive data? There is a better way to go. Prog. Neurobiol. 1994, 44:233-247.
46. Oorschot D.E. Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigral nuclei of the rat basal ganglia: a stereological study using the Cavalieri and optical disector methods. J. Comp. Neurol. 1996, 366:580-599.
47. Oorschot D.E. Indirect measures of neuroprotection are parameters to avoid: examples from research on neonatal rat hypoxia-ischemia. Image Anal. Stereol. 2011, 30:1-9.
48. Oorschot D.E. The percentage of interneurons in the dorsal striatum of the rat, cat, monkey and human: a critique of the evidence. Basal Ganglia 2013, 3:19-24.
49. Oorschot D.E., Tunstall M.J., Wickens J.R. Local connectivity between striatal spiny projection neurons: a re-evaluation. The Basal Ganglia VII 2002, 421-434. Kluwer Academic/Plenum Publishers, New York. L.F.B. Nicholson, R.L.M. Faull (Eds.).
50. Oorschot D.E., Lin N., Cooper B.H., Reynolds J.N.J., Sun H., Wickens J.R. Synaptic connectivity between rat striatal spiny projection neurons in vivo: unexpected multiple somatic innervation in the context of overall sparse proximal connectivity. Basal Ganglia 2013, 3:93-108.
51. Oorschot D.E., Voss L., Covey M.V., Goddard L., Huang W., Birchall P., Bilkey D.K., Kohe S.E. Spectrum of short- and long-term brain pathology and long-term behavioral deficits in male repeated hypoxic rats closely resembling human extreme prematurity. J. Neurosci. 2013, 33:11863-11877.
52. Ouimet C.C., Langley-Gullion K.C., Greengard P. Quantitative immunocytochemistry of DARPP-32-expressing neurons in the rat caudatoputamen. Brain Res. 1998, 808:8-12.
53. Paxinos G., Watson C. The Rat Brain in Stereotaxic Co-ordinates 2007, Academic Press, Amsterdam. Sixth ed.
54. Perlman J.M. Summary proceedings from the neurology group on hypoxic-ischemic encephalopathy. Pediatrics 2006, 117:S28-S33.
55. Plane J.M., Liu R., Wang T.-W., Silverstein F.S., Parent J.M. Neonatal hypoxic-ischemic injury increases forebrain subventricular zone neurogenesis in the mouse. Neurobiol. Dis. 2004, 16:585-595.
56. Price A.W., Fowler S.C. Deficits in contralateral and ipsilateral forepaw motor control following unilateral motor cortical ablations in rats. Brain Res. 1981, 205:81-90.
57. Raadsheer F.C., Oorschot D.E., Verwer R.W.H., Tilders F.J.H., Swaab D.F. Age-related increase in the total number of corticotropin-releasing hormone neurons in the human paraventricular nucleus in controls and Alzheimer's Disease: comparison of the disector with an unfolding method. J. Comp. Neurol. 1994, 339:447-457.
58. Rakic P. Adult neurogenesis in mammals: an identity crisis. J. Neurosci. 2002, 22:614-618.
59. Rice J.E., Vannucci R.C., Brierley J.B. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 1981, 9:131-141.
60. Rosenkranz K., Kumbruch S., Lebermann K., Marschner K., Jensen A., Dermietzel R., Meier C. The chemokine SDF-1/CXCL12 contributes to the 'homing' of umbilical cord blood cells to a hypoxic-ischemic lesion in the rat brain. J. Neurosci. Res. 2010, 88:1223-1233.
61. Schallert T., Fleming S.M., Leasure J.L., Tillerson J.L., Bland S.T. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 2000, 39:777-787.
62. Slomianka L., West M.J. Estimators of the precision of stereological estimates: an example based on the CA1 pyramidal cell layer of rats. Neurosciences 2005, 136:757-767.
63. Sun X., Zhang Q.W., Xu M., Guo J.J., Shen S.W., Wang Y.Q., Sun F.Y. New striatal neurons form projections to substantia nigra in adult rat brain after stroke. Neurobiol. Dis. 2012, 45:601-609.
64. Tattersfield A.S., Croon R.J., Liu Y.W., Kells A.P., Faull R.L.M., Connor B. Neurogenesis in the striatum of the quinolinic acid lesion model of Huntington's disease. Neurosciences 2004, 127:319-332.
65. Tavazoie M., Van der Veken L., Silva-Vargas V., Louissaint M., Colonna L., Zaidi B., Garcia-Verdugo J.M., Doetsch F. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008, 3:279-288.
66. Titomanlio L., Kavelaars A., Dalous J., Mani S., El Ghouzzi V., Heijnen C., Baud O., Gressens P. Stem cell therapy for neonatal brain injury: perspectives and challenges. Ann. Neurol. 2011, 70:698-712.
67. Tuor U.I., Hudzik T.J., Malisza K., Sydserff S., Kozlowski P., Del Bigio M.R. Long-term deficits following cerebral hypoxia-ischemia in four-week-old rats: correspondence between behavioral, histological, and magnetic resonance imaging assessments. Exp. Neurol. 2001, 167:272-281.
68. Uccelli A. Mesenchymal stem cells exert a remarkable regenerative effect requiring minimal CNS integration. Exp. Neurol. 2013, 247:292-295.
69. van Velthoven C.T.J., Kavelaars A., van Bel F., Heijnen C.J. Mesenchymal stem cell treatment after neonatal hypoxic-ischemic brain injury improves behavioral outcome and induces neuronal and oligodendrocyte regeneration. Brain Behav. Immun. 2010, 24:387-393.
70. van Velthoven C.T.J., Kavelaars A., van Bel F., Heijnen C.J. 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. 2010, 30:9603-9611.
71. van Velthoven C.T.J., Kavelaars A., van Bel F., Heijnen C.J. Nasal administration of stem cells: a promising novel route to treat neonatal ischemic brain damage. Pediatr. Res. 2010, 68:419-422.
72. van Velthoven C.T.J., Kavelaars A., van Bel F., Heijnen C.J. Mesenchymal stem cell transplantation changes the gene expression profile of the neonatal ischemic brain. Brain Behav. Immun. 2011, 25:1342-1348.
73. van Velthoven C.T.J., Kavelaars A., Heijnen C.J. Mesenchymal stem cells as a treatment for neonatal ischemic brain damage. Pediatr. Res. 2012, 71:474-481.
74. Volpe J.J. Perinatal hypoxic-ischemic brain injury: overview. Fetal and Perinatal Neurology 1992, 232-252. Karger, Tokyo. Y. Fukuyama, Y. Suzuki, S. Kamoshita, P. Casaer (Eds.).
75. Wang Y., Deng Y., Zhou G.-Q. SDF-1[alpha]/CXCR4-mediated migration of systemically transplanted bone marrow stromal cells towards ischemic brain lesion in a rat model. Brain Res. 2008, 1195:104-112.
76. West M.J., Gundersen H.J.G. Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 1990, 296:1-22.
77. Williams M.A. Quantitative methods in biology. Practical Methods in Electron Microscopy, Volume 6 1977, North Holland Publishing Company, Amsterdam. A.M. Glauert (Ed.).
78. Williams C.G., Kim T.K., Taboas A., Malik A., Manson P., Elisseeff J. In vitro chondrogenesis of bone marrow-derived mesenchymal stem cells in a photopolymerizing hydrogel. Tissue Eng. 2003, 9:679-688.
79. Willing A., Foran E.A. Cord blood as a treatment for stroke. Cellular Therapy for Stroke and CNS Injuries 2015, Springer. L.-R. Zhao, J.H. Zhang (Eds.).
80. Wilson T., Stark C., Holmbom J., Rosling A., Kuusilehto A., Tirri T., Penttinen R., Ekholm E. Fate of bone marrow-derived stromal cells after intraperitoneal infusion of implantation into femoral bone defects in the host animal. J. Tissue Eng. 2010, 10.4061/2010/345806.
81. Yang Z., Levison S.W. Hypoxia/ischemia expands the regenerative capacity of progenitors in the perinatal subventricular zone. Neurosci. 2006, 139:555-564.
82. Yang Z., Levison S.W. Perinatal hypoxic/ischemic brain injury induces persistent production of striatal neurons from subventricular zone progenitors. Dev. Neurosci. 2007, 29:331-340.
83. Yang Z., You Y., Levison S.W. Neonatal hypoxic/ischemic brain injury induces production of calretinin-expressing interneurons in the striatum. J. Comp. Neurol. 2008, 511:19-33.
84. Yoshikawa G., Momiyama T., Oya S., Takai K., Tanaka J., Higashiyama S., Saito N., Kirino T., Kawahara N. Induction of striatal neurogenesis and generation of region-specific functional mature neurons after ischemia by growth factors. J. Neurosurg. 2010, 113:835-850.