Multiple intravenous administrations of human umbilical cord blood cells benefit in a mouse model of ALS

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Garbuzova Davis, Svitlana ^a   Rodrigues, Maria C O ^a,c   Mirtyl, Santhia ^a   Turner, Shanna ^a   Mitha, Shazia ^a   Sodhi, Jasmine ^a   Suthakaran, Subatha ^a   Eve, David J ^a   Sanberg, Cyndy D ^b   Kuzmin Nichols, Nicole ^b   Sanberg, Paul R ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b Saneron CCEL Therapeutics Inc   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DENSITY; CONTROLLED STUDY; CORD BLOOD STEM CELL TRANSPLANTATION; DISEASE COURSE; GLIA CELL; IMMUNOHISTOCHEMISTRY; LIFESPAN; MICROGLIA; MOTOR PERFORMANCE; MOUSE; NONHUMAN; TREATMENT RESPONSE; ANIMAL; DISEASE MODEL; FETUS BLOOD; HUMAN; INTRAVENOUS DRUG ADMINISTRATION; MOTONEURON; TRANSPLANTATION; TREATMENT OUTCOME;

MUS;

AUTACOID;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; DISEASE MODELS, ANIMAL; FETAL BLOOD; HUMANS; INFLAMMATION MEDIATORS; INFUSIONS, INTRAVENOUS; MICE; MOTOR NEURONS; TREATMENT OUTCOME;

EID: 84856557925     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031254     Document Type: Article

References (76)

1. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, et al. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyothrophic lateral sclerosis. Nature 362: 59-62.
2. Bruijn LI, (2002) Amyotrophic lateral sclerosis: from disease mechanisms to therapies. Biotechniques 32: 1112-1116.
3. Cleveland DW, Rothstein JD, (2001) From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2: 806-819.
4. Strong MJ, (2003) The basic aspects of therapeutics in amyotrophic lateral sclerosis. Pharmacol Ther 98: 379-414.
5. Garbuzova-Davis S, Rodrigues MC, Hernandez-Ontiveros DG, Louis MK, Willing AE, et al. (2011) Amyotrophic Lateral Sclerosis: A neurovascular disease. Brain Res 1398: 113-125.
6. Garbuzova-Davis S, Sanberg PR, (2009) Feasibility of cell therapy for amyotrophic lateral sclerosis. Exp Neurol 216: 3-6.
7. Riley J, Sweeney W, Boulis N, (2008) Shifting the balance: cell-based therapeutics as modifiers of the amyotrophic lateral sclerosis-specific neuronal microenvironment. Neurosurg Focus 24: E10.
8. Suzuki M, Svendsen CN, (2008) Combining growth factor and stem cell therapy for amyotrophic lateral sclerosis. Trends Neurosci 31: 192-198.
9. Appel SH, Simpson EP, (2001) Activated microglia: the silent executioner in neurodegenerative disease? Curr Neurol Neurosci Rep 1: 303-305.
10. Henkel JS, Beers DR, Zhao W, Appel SH, (2009) Microglia in ALS: the good, the bad, and the resting. J Neuroimmune Pharmacol 4: 389-398.
11. Zhao W, Beers DR, Henkel JS, Zhang W, Urushitani M, et al. (2010) Extracellular mutant SOD1 induces microglial-mediated motoneuron injury. Glia 58: 231-243.
12. Lindvall O, Kokaia Z, Martinez-Serrano A, (2004) Stem cell therapy for human neurodegenerative disorders- how to make it work. Nat Med 10: S42-S50.
13. Eglitis MA, Dawson D, Park KW, Mouradian MM, (1999) Targeting of marrow-derived astrocytes to the ischemic brain. NeuroReport 10: 1289-1292.
14. Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, et al. (1998) Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279: 1528-1530.
15. Prockop DJ, (1997) Marrow stromal cells as stem cells for non hematopoietic tissues. Science 276: 71-74.
16. Sanchez-Ramos J, Song S, Cardozo-Pelaez F, Hazzi C, Stedeford T, et al. (2000) Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol 164: 247-256.
17. Teng YD, Yu D, Ropper AW, Li J, Kabatas S, et al. (2011) Functional multipotency of stem cells: a conceptual review of neuroprophic factor-based evidance and its role in translational research. Curr Neuropharmacol 9: 574-585.
18. Mazzini L, Fagioli F, Boccaletti R, Mareschi K, Oliveri C, et al. (2003) Stem cell therapy in amyotrophic lateral sclerosis: a methodological approach in humans. Amyotroph Lateral Scler Other Motor Neuron Disord 4: 158-161.
19. Mazzini L, Mareschi K, Ferrero I, Vassallo E, Oliveri G, et al. (2008) Stem cell treatment in Amyotrophic Lateral Sclerosis. J Neurol Sci 265: 78-83.
20. Appel SH, Engelhardt JI, Henkel JS, Siklos L, Beers DR, et al. (2008) Hematopoietic stem cell transplantation in patients with sporadic amyotrophic lateral sclerosis. Neurology 71: 1326-1334.
21. Garbuzova-Davis S, Willing AE, Saporta S, Bickford PC, Gemma C, et al. (2006) Novel cell therapy approaches for brain repair. Prog Brain Res 157: 207-222.
22. Sanberg PR, Willing AE, Cahill DW, (2001) Neurosurgery for the 21st century. What does neurobiology justify for repairing neurodegenerative disorders? Clin Neurosurg 48: 113-126.
23. Sanberg PR, Willing AE, Cahill DW, (2002) Novel cellular approaches to repair of neurodegenerative disease: from Sertoli cells to umbilical cord blood stem cells. Neurotox Res 4: 95-101.
24. Sanberg PR, Willing AE, Garbuzova-Davis S, Saporta S, Liu G, et al. (2005) Umbilical cord blood-derived stem cells and brain repair. Ann NY Acad Sci 1049: 67-83.
25. Sanberg PR, Eve DJ, Willing AE, Tan J, Sanberg CD, et al. (2011) The treatment of neurodegenerative disorders using umbilical cord and menstrual blood-derived stem cells. Cell Transplant 20: 85-94.
26. Broxmeyer HE, Douglas GW, Hangoc G, Cooper S, Bard J, et al. (1989) Human umbilical cord blood as a potential source of transplantable hematopoietic stem/progenitor cells. Proc Natl Acad Sci U S A 86: 3828-3832.
27. Broxmeyer HE, Hangoc G, Cooper S, Ribeiro RC, Graves V, et al. (1992) Growth characteristics and expansion of human umbilical cord blood and estimation of its potential for transplantation in adults. Proc Natl Acad Sci U S A 89: 4109-4113.
28. Mayani H, Lansdorp PM, (1998) Biology of human umbilical cord blood hematopoietic stem/progenitor cells. Stem Cells 16: 153-165.
29. Nakahata T, Ogawa M, (1982) Hemopoietic colony-forming cells in umbilical cord blood with extensive capability to generate mono- and multipotential hemopoietic progenitors. J Clin Invest 70: 1324-1328.
30. Nayar B, Raju GM, Deka D, (2002) Hematopoietic stem/ progenitor cell harvesting from umbilical cord blood. Int J Gynaecol Obstet 79: 31-32.
31. Todaro AM, Pafumi C, Pernicone G, Munda S, Pilastro MR, et al. (2000) Haematopoietic progenitors from umbilical cord blood. Blood Purif 18: 144-147.
32. Chen N, Hudsion JE, Walczak P, Misiuta I, Garbuzova-Davis S, et al. (2005) Human umbilical cord blood progenitors: the potential of these hematopoietic cells to become neural. Stem Cells 23: 1560-1570.
33. Sanchez-Ramos JR, Song S, Kamath SG, Zigova T, Willing A, et al. (2001) Expression of neural markers in human umbilical cord blood. Exp Neurol 171: 109-115.
34. Sanchez-Ramos JR, (2002) Neural cells derived from adult bone marrow and umbilical cord blood. Neurosci Res 69: 880-893.
35. Zola H, Fusco M, Macardle PJ, Flego L, Roberton D, (1995) Expression of cytokine receptors by human cord blood lymphocytes: comparison with adult blood lymphocytes. Pediatr Res 38: 397-403.
36. Rainsford E, Reen DJ, (2002) Interleukin 10, produced in abundance by human newborn T cell, may be the regulator of increased tolerance associated with cord blood stem cell transplantation. Br J Haematol 116: 702-709.
37. Chen N, Newcomb J, Garbuzova-Davis S, Davis Sanberg C, Sanberg PR, et al. (2010) Human umbilical cord blood cells have trophic effects on young and aging hippocampal neurons in vitro. Aging Dis 1: 173-190.
38. Chen J, Sanberg PR, Li Y, Wang L, Lu M, et al. (2001) Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats. Stroke 32: 2682-2688.
39. Vendrame M, Gemma C, de Mesquita D, Collier L, Bickford PC, et al. (2005) Anti-inflammatory effects of human cord blood cells in a rat model of stroke. Stem Cells Dev 14: 595-604.
40. Willing AE, Jiang L, Milliken M, Poulos S, Zigova T, et al. (2003) Intravenous versus intrastriatal cord blood administration in a rodent model of stroke. J Neurosci Res 73: 296-307.
41. Lu D, Sanberg PR, Mahmood A, Li Y, Wang L, et al. (2002) Intravenous administration of human umbilical cord blood reduces neurological deficit in the rat after traumatic brain injury. Cell Transplant 11: 275-281.
42. Saporta S, Kim JJ, Willing AE, Fu ES, Hart CD, et al. (2003) Intravenous administration of human umbilical cord blood cells in rats with spinal cord injury. J Hematother Stem Cell Res 12: 271-278.
43. Nikolic W, Hou H, Town T, Zhu Y, Giunta B, et al. (2008) Peripherally administered human umbilical cord blood cells reduce parenchymal and vascular beta-amyloid deposits in Alzheimer mice. Stem Cells Dev 17: 423-440.
44. Bachstetter A, Pabon MM, Cole MJ, Hudson CE, Sanberg PR, et al. (2008) Peripheral injection of human umbilical cord blood stimulates neurogenesis in the aged rat brain. BMC Neurosci 9: 22.
45. Garbuzova-Davis S, Willing AE, Zigova T, Saporta S, Justen EB, et al. (2003) Intravenous administration of human umbilical cord blood cells in a mouse model of amyotrophic lateral sclerosis: distribution, migration, and differentiation. Hematother Stem Cell Res 12: 255-270.
46. Garbuzova-Davis S, Sanberg CD, Kuzmin-Nichols N, Willing AE, Gemma C, et al. (2008) Human umbilical cord blood treatment in a mouse model of ALS: optimization of cell dose. PLoS ONE 3: e2494.
47. Freireich EJ, Gehan EA, Rall DP, Schmidt LH, Skipper HE, (1966) Quantitative comparison of toxicity of anticancer agents in mouse, rat, hamster, dog, monkey, and man. Cancer Chemother Rep 50: 219-244.
48. Chen R, Ende N, (2000) The potential for the use of mononuclear cells from human umbilical cord blood in the treatment of amyotrophic lateral sclerosis in SOD1 mice. J Med 31: 21-30.
49. Rizvanov AA, Kiyasov AP, Gaziziov IM, Yilmaz TS, Kaligin MS, et al. (2008) Human umbilical cord blood cells transfected with VEGF and L(1)CAM do not differentiate into neurons but transform into vascular endothelial cells and secrete neuro-trophic factors to support neuro-genesis-a novel approach in stem cell therapy. Neurochem Int 53: 389-394.
50. Alexianu ME, Kozovska M, Appel SH, (2001) Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology 57: 1282-1289.
51. Feeney SJ, McKelvie PA, Austin L, Jean-Francois MJ, Kapsa R, et al. (2001) Presymptomatic motor neuron loss and reactive astrocytosis in the SOD1 mouse model of amyotrophic lateral sclerosis. Muscle Nerve 24: 1510-1519.
52. Hall ED, Oostveen JA, Gurney ME, (1998) Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 23: 249-256.
53. Philips T, Robberecht W, (2011) Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease. Lancet Neurol 10: 253-263.
54. Garbuzova-Davis S, Xie Y, Zayko O, Sanberg PR, (2009) Human umbilical cord blood cells in treatment of Sanfilippo syndrome type B. Cell Transplant 18: 214-215.
55. Jozwiak S, Habich A, Kotulska K, Samowska A, Kropiwnicki T, et al. (2010) Intracerebroventricular transplantation of cord blood-derived neural progenitors in a child with severe global brain ischemic injury. Cell Med, Part B of Cell Transplant 1: 71-80.
56. Ohnishi S, Ito H, Suzuki Y, Adachi Y, Wate R, et al. (2009) Intra-bone marrow-bone marrow transplantation slows disease progression and prolongs survival in G93A SOD1 transgenic mice, an animal model mouse of amyotrophic lateral sclerosis. Brain Res 1296: 216-224.
57. Van Den Bosch L, Robberecht W, (2008) Crosstalk between astrocytes and motor neurons: What is the message? Exp Neurol 211: 1-6.
58. Boillée S, Velde CV, Cleveland DW, (2006) ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52: 39-59.
59. Yamanaka K, Chun SJ, Boillee S, Fujimori-Tonou N, Yamashita H, et al. (2008) Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci 11: 251-253.
60. Boillée S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, et al. (2006) Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312: 1389-1392.
61. Cho KJ, Chung YH, Shin C, Shin DH, Kim YS, et al. (1999) Reactive astrocytes express p53 in the spinal cord of transgenic mice expressing a human Cu/Zn SOD mutation. Neuro Report 10: 3939-3943.
62. Henkel JS, Engelhardt JI, Siklós L, Simpson EP, Kim SH, et al. (2004) Presence of dendritic cells, MCP-1, and activated microglia/macrophages in amyotrophic lateral sclerosis spinal cord tissue. Ann Neurol 55: 221-235.
63. Levine JB, Kong J, Nadler M, Xu Z, (1999) Astrocytes interact intimately with degenerating motor neurons in mouse amyotrophic lateral sclerosis (ALS). Glia 28: 215-224.
64. McGeer PL, McGeer EG, (2002) Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve 26: 459-470.
65. Barbeito LH, Pehar M, Cassina P, Vargas MR, Peluffo H, et al. A role for astrocytes in motor neuron loss in amyotrophic lateral sclerosis. Brain Res Brain Res Rev 47: 263-274.
66. Di Giorgio FP, Carrasco MA, Siao MC, Maniatis T, Eggan K, (2007) Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat Neurosci 10: 608-614.
67. Giulian D, Baker TJ, (1985) Peptides releasing by ameboid microglia regulate astroglial proliferation. J Cell Biol 101: 2411-2415.
68. Hendrikx PJ, Martens CM, Hagenbeek A, Keij JF, Visser JW, (1996) Homing of fluorescently labeled murine hematopoietic stem cells. Exp Hematol 24: 129-140.
69. Szilvassy SJ, Bass MJ, Van Zant G, Grimes B, (1999) Organ-selective homing defines engraftment kinetics of murine hematopoietic stem cells and is compromised by ex vivo expansion. Blood 93: 1557-1566.
70. Lee ST, Chu K, Jung KH, Kim SJ, Kim DH, et al. (2008) Anti-inflammatory mechanism of intravascular neural stem cell transplantation in haemorrhagic stroke. Brain 131: 616-629.
71. Souayah N, Coakley KM, Chen R, Ende N, McArdle JJ, (2011) Defective Neuromuscular transmission in the SOD1(G93A) transgenic mouse improves after administration of human umbilical cord blood cells. Stem Cell Rev [In press] DOI: 10.1007/s12015-011-9281-3.
72. Mitrecic D, Nicaise C, Gajovic S, Pochet R, (2010) Distribution, differentiation, and survival of intravenously administered neural stem cells in a rat model of amyotrophic lateral sclerosis. Cell Transplant 19: 537-548.
73. Borlongan CV, Hadman M, Sanberg CD, Sanberg PR, (2004) Central nervous system entry of peripherally injected umbilical cord blood cells is not required for neuroprotection in stroke. Stroke 35: 2385-2389.
74. Heiman-Patterson TD, Deitch JS, Blankenhorn EP, Erwin KL, Perreault MJ, et al. (2005) Background and gender effects on survival in the TgN(SOD1-G93A)1Gur mouse model of ALS. J Neurol Sci 236: 1-7.
75. Alexander GM, Erwin KL, Byers N, Deitch JS, Augelli BJ, et al. (2004) Effect of transgene copy number on survival in the G93A SOD1 transgenic mouse model of ALS. Brain Res Mol Brain Res 130: 7-15.
76. West MJ, Slomianka L, Gundersen HJ, (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231: 482-497.