Intracerebroventricular administration of human umbilical cord blood cells delays disease progression in two murine models of motor neuron degeneration

Rejuvenation Research

Volumn 14, Issue 6, 2011, Pages 623-639

  Bigini, P ^a   Veglianese, P ^a   Andriolo, G ^b   Cova, L ^c   Grignaschi, G ^a   Caron, I ^a   Daleno, C ^a   Barbera, S ^a   Ottolina, A ^a   Calzarossa, C ^c   Lazzari, L ^b   Mennini, T ^a   Bendotti, C ^a   Silani, V ^c  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^c ISTITUTO AUXOLOGICO ITALIANO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BRAIN VENTRICLE; CELL THERAPY; CELL TRANSPLANTATION; CENTRAL NERVOUS SYSTEM; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; DISEASE COURSE; FEMALE; HUMAN; HUMAN CELL; LIFESPAN; MALE; MONONUCLEAR CELL; MOTOR NEURON DISEASE; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SPINAL CORD VENTRAL HORN; SURVIVAL; UMBILICAL CORD BLOOD;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BISBENZIMIDAZOLE; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FETAL BLOOD; HUMANS; INFANT, NEWBORN; INFUSIONS, INTRAVENTRICULAR; MICE; MICE, TRANSGENIC; MOTOR NEURON DISEASE; POLYMERASE CHAIN REACTION; SPINAL CORD; TISSUE THERAPY;

EID: 83755225754     PISSN: 15491684     EISSN: 15578577     Source Type: Journal    
DOI: 10.1089/rej.2011.1197     Document Type: Article

References (71)

1. Eve DJ, Sanberg PR. Stem cell research in Cell Transplantation: An analysis of geopolitical influence by publications. Cell Transplant 2007;16:867-873. (Pubitemid 351448262)
2. Harris DT. Cord blood stem cells: A review of potential neurological applications. Stem Cell Rev 2008;4:269-274.
3. Silani V, Corbo M. Cell-replacement therapy with stem cells in neurodegenerative diseases. Curr Neurovasc Res 2004;1: 283-289.
4. Herranz AS, Gonzalo-Gobernado R, Reimers D, Asensio MJ, Rodriguez-Serrano M, Bazan E. Applications of human umbilical cord blood cells in central nervous system regeneration. Curr Stem Cell Res Ther 2009;5:17-22.
5. Tse W, Bunting KD. The expanding tool kit for hematopoietic stem cell research. Methods Mol Biol 2008;430:3-18.
6. Park DH, Lee JH, Borlongan CV, Sanberg PR, Chung YG, Cho TH. Transplantation of umbilical cord blood stem cells for treating spinal cord injury. Stem Cell Rev 2010;7:181-194.
7. Ende N, Chen R. Human umbilical cord blood cells ameliorate Huntington's disease in transgenic mice. J Med 2001; 32:231-240. (Pubitemid 32899515)
8. Ende N, Chen R, Ende-Harris D. Human umbilical cord blood cells ameliorate Alzheimer's disease in transgenic mice. J Med 2001;32:241-247. (Pubitemid 32899516)
9. Ende N, Weinstein F, Chen R, Ende M. Human umbilical cord blood effect on sod mice (amyotrophic lateral sclerosis). Life Sci 2000;67:53-59. (Pubitemid 30368622)
10. Chen R, Ende N. 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 2000; 31:21-30. (Pubitemid 30614798)
11. Garbuzova-Davis S, Sanberg CD, Kuzmin-Nichols N, Willing AE, Gemma C, Bickford PC, Miller C, Rossi R, Sanberg PR. Human umbilical cord blood treatment in a mouse model of ALS: optimization of cell dose. PLoS One 2008; 3:e2494.
12. Garbuzova-Davis S, Sanberg PR. Feasibility of cell therapy for amyotrophic lateral sclerosis. Exp Neurol 2009;216:3-6.
13. Garbuzova-Davis S, Willing AE, Zigova T, Saporta S, Justen EB, Lane JC, Hudson JE, Chen N, Davis CD, Sanberg PR. Intravenous administration of human umbilical cord blood cells in a mouse model of amyotrophic lateral sclerosis: Distribution, migration, and differentiation. J Hematother Stem Cell Res. 2003;12:255-270. (Pubitemid 36736737)
14. Corti S, Locatelli F, Papadimitriou D, Del Bo R, Nizzardo M, Nardini M, Donadoni C, Salani S, Fortunato F, Strazzer S, Bresolin N, Comi GP. Neural stem cells LewisX + CXCR4 + modify disease progression in an amyotrophic lateral sclerosis model. Brain 2007;130:1289-1305. (Pubitemid 47355948)
15. Nicaise C, Mitrecic D, Pochet R. Brain and spinal cord affected by amyotrophic lateral sclerosis induce differential growth factors expression in rat mesenchymal and neural stem cells. Neuropathol Appl Neurobiol 2010;37:179-188.
16. Schmitt-John T, Drepper C, Mussmann A, Hahn P, Kuhlmann M, Thiel C, Hafner M, Lengeling A, Heimann P, Jones JM, Meisler MH, Jockusch H. Mutation of Vps54 causes and defective spermiogenesis in the wobbler mouse. Nat Genet 2005;37:1213-1215. (Pubitemid 41568703)
17. Heiman-Patterson TD, Deitch JS, Blankenhorn EP, Erwin KL, Perreault MJ, Alexander BK, Byers N, Toman I, Alexander GM. Background and gender effects on survival in the TgN(SOD1-G93A)1Gur mouse model of ALS. J Neurol Sci 2005;236:1-7. (Pubitemid 41218685)
18. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Den H-X, Rahmani Z, Krizus A, McKenna-Yasek D, Cayabyab A, Gaston SM, Berger R, Tanzi RE, Halperin JJ, Herzfeldt B, Van den Bergh R, Hung W-Y, Bird T, Deng G, Mulder DW, Smyth C, Laing NG, Soriano E, Pericak-Vance MA, Haines J, Rouleau GA, Gusella JS, Horvitz HR, Brown RH Jr. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993;362:59-62. (Pubitemid 23087289)
19. Rathke-Hartlieb S, Schmidt VC, Jockusch H, Schmitt-John T, Bartsch JW. Spatiotemporal progression of neurodegeneration and glia activation in the wobbler neuropathy of the mouse. Neuroreport 1999;10:3411-3416.
20. Bigini P, Atzori C, Fumagalli E, Cagnotto A, Barbera S, Migheli A, Mennini T. Lack of caspase-dependent apoptosis in spinal motor neurons of the wobbler mouse. Neurosci Lett 2007;426:106-110. (Pubitemid 47464708)
21. Houser CR, Crawford GD, Barber RP, Salvaterra PM, Vaughn JE. Organization and morphological characteristics of cholinergic neurons: An immunocytochemical study with a monoclonal antibody to choline acetyltransferase. Brain Res 1983;266:97-119. (Pubitemid 13117581)
22. Tortarolo M, Grignaschi G, Calvaresi N, et al. Glutamate AMPA receptors change in motor neurons of SOD1G93A transgenic mice and their inhibition by a noncompetitive antagonist ameliorates the progression of amytrophic lateral sclerosis-like disease. J Neurosci Res 2006;83:134-146. (Pubitemid 43062017)
23. Storkebaum E, Lambrechts D, Dewerchin M, Moreno-Muciano M-P, Appelmans S, Oh H, Van Damme P, Rutten B, Man WY, De Mol M, Wyns S, Manka D, Vermeulen K, Van Den Bosch L, Mertens N, Schmitz C, Robberecht W, Conway EM, Collen D, Moons L, Carmellet P. Treatment of motoneuron degeneration by intracerebroventricular delivery of VEGF in a rat model of ALS. Nat Neurosci 2005;8:85-92. (Pubitemid 41236736)
24. Guyton AC, Hall JE. Cerebral blood flow, the cerebrospinal fluid, and brain metabolism. In: Guyton AC, Hall JE (eds). Textbook of Medical Physiology, 10th ed. W.B. Saunders, Philadelphia, 2000, pp 704-716.
25. Gould TW, Buss RR, Vinsant S, Prevette D, Sun W, Knudson CM, Milligan CE, Oppenheim RW. Complete dissociation of motor neuron death from motor dysfunction by Bax deletion in a mouse model of ALS. J Neurosci 2006;26:8774-8786. (Pubitemid 44319413)
26. Suzuki M, McHugh J, Tork C, Shelley B, Klein SM, Aebischer P, Svendsen CN. GDNF secreting human neural progenitor cells protect dying motor neurons, but not their projection to muscle, in a rat model of familial ALS. PLoS ONE 2007;2:e689.
27. Souayah N, Coakley KM, Chen R, Ende N, McArdle JJ. Defective neuromuscular transmission in the SOD1(G93A) transgenic mouse improves after administration of human umbilical cord blood cells. Stem Cell Rev DOI: 10.1007/s12015-011-9281-3.
28. Fischer LR, Glass JD. Axonal degeneration in motor neuron disease. Neurodegener Dis 2007;4:431-442. (Pubitemid 47557285)
29. Fan CG, Zhang QJ, Tang FW, Han ZB, Wang GS, Han ZC. Human umbilical cord blood cells express neurotrophic factors. Neurosci Lett 2005;380:322-325.
30. Newman MB, Willing AE, Manresa JJ, Sanberg CD, Sanberg PR. Cytokines produced by cultured human umbilical cord blood (HUCB) cells: Implications for brain repair. Exp Neurol 2006;199:201-208.
31. Chou DL, Daugherty BL, McKenna EK, Hsu WM, Tyler NK, Plopper CG, Hyde DM, Schelegle ES, Gershwin LJ, Miller LA. Chronic aeroallergen during infancy enhances eotaxin-3 expression in airway epithelium and nerves. Am J Respir Cell Mol Biol 2005;33:1-8. (Pubitemid 40961007)
32. Fulkerson PC, Fischetti CA, McBride ML, Hassman LM, Hogan SP, Rothenberg ME. A central regulatory role for eosinophils and the eotaxin/CCR3 axis in chronic experimental allergic airway inflammation. Proc Natl Acad Sci USA 2006;103:16418-16423. (Pubitemid 44715211)
33. Wainwright DA, Mesnard NA, Xin J, Sanders VM, Jones KJ. Effects of facial nerve axotomy on Th2-associated and Th1-associated chemokine mRNA expression in the facial motor nucleus of wild-type and presymptomatic SOD1 mice. J Neurodegener Regen 2009;2:39-44.
34. Kuhle J, Lindberg RL, Regeniter A, Mehling M, Steck AJ, Kappos L, Czaplinski A. Increased levels of inflammatory chemokines in amyotrophic lateral sclerosis. Eur J Neurol 2009;16:771-774.
35. Garbuzova-Davis S, Saporta S, Sanberg PR. Implications of blood-brain barrier disruption in ALS. Amyotroph Lateral Scler 2008;9:375-376.
36. Banerjee R, Mosley RL, Reynolds AD, Dhar A, Jackson-Lewis V, Gordon PH, Przedborski S, Gendelman HE. Adaptive immune neuroprotection in G93A-SOD1 amyotrophic lateral sclerosis mice. PLoS One 2008;3:e2740.
37. Chiu IM, Chen A, Zheng Y, Kosaras B, Tsiftsoglou SA, Vartanian TK, Brown RH JR, Carroll MC. T lymphocytes potentiate endogenous neuroprotective inflammation in a mouse model of ALS. Proc Natl Acad Sci USA 2008;105: 17913-17918.
38. Appel SH, Beers DR, Henkel JS. T cell-microglial dialogue in Parkinson's disease and amyotrophic lateral sclerosis: are we listening? Trends Immunol 2010 31 7-17.
39. Kadoyama K, Funakoshi H, Ohya W, Nakamura T. Hepatocyte growth factor (HGF) attenuates gliosis and motoneuronal degeneration in the brainstem motor nuclei of a transgenic mouse model of ALS. Neurosci Res 2007;59: 446-456. (Pubitemid 350007815)
40. Sun W, Funakoshi H, Nakamura T. Overexpression of HGF retards disease progression and prolongs life span in a transgenic mouse model of ALS. J Neurosci 2002;22:6537-6548. (Pubitemid 35386410)
41. Kato S, Funakoshi H, Nakamura T, Kato M, Nakano I, Hirano A, Ohama E. Expression of hepatocyte growth factor and c-Met in the anterior horn cells of the spinal cord in the patients with amyotrophic lateral sclerosis (ALS): Immunohistochemical studies on sporadic ALS and familial ALS with superoxide dismutase 1 gene mutation. Acta Neuropathol 2003;106:112-120. (Pubitemid 36869244)
42. Henkel JS, Beers DR, Siklos L, Appel SH. The chemokine MCP-1 and the dendritic and myeloid cells it attracts are increased in the mSOD1 mouse model of ALS. Mol Cell Neurosci 2006;31:427-437. (Pubitemid 43358017)
43. Grumbles RM, Casella GT, Rudinsky MJ, Wood, PM, Sesodia S, Bent M, Thomas CK. Long-term delivery of FGF-6 changes the fiber type and fatigability of muscle reinnervated from embryonic neurons transplanted into adult rat peripheral nerve. J Neurosci Res 2007;85:1933-1942. (Pubitemid 47051481)
44. Uchida K, Nakajima H, Inukai T, Takamura T, Kobayashi S, Furukawa S, Baba H. Adenovirus-mediated retrograde transfer of neurotrophin-3 gene enhances survival of anterior horn neurons of twy/twy mice with chronic mechanical compression of the spinal cord. J Neurosci Res 2008;86: 1789-1800. (Pubitemid 351859429)
45. Ikeda K, Iwasaki Y, Shiojima T, Kinoshita M. Neuroprotective effect of various cytokines on developing spinal motoneurons following axotomy. J Neurol Sci 1996;135: 109-113. (Pubitemid 26072588)
46. Henning RJ, Burgos JD, Vasko M, Alvarado F, Sanberg CD, Sanberg PR, Morgan MB. Human cord blood cells and myocardial infarction: Effect of dose and route of administration on infarct size. Cell Transplant 2007;16:907-917. (Pubitemid 351448608)
47. Ali O, Cohen P, Lee KW. Epidemiology and biology of insulin-like growth factor binding protein-3 (IGFBP-3) as an anti-cancer molecule. Horm Metab Res 2003;35:726-733. (Pubitemid 38058176)
48. Amerio P, Frezzolini A, Feliciani C, Verdolini R, Teofoli P, De Pita O, Puddu P. Eotaxins and CCR3 receptor in inflammatory and allergic skin diseases: Therapeutical implications. Curr Drug Targets Inflamm Allergy 2003;2:81-94.
49. Armand AS, Laziz I, Chanoine C. FGF6 in myogenesis. Biochim Biophys Acta 2006;1763:773-778. (Pubitemid 44205279)
50. Ebadi M, Bashir RM, Heidrick ML, Hamada FM, El Refaeyet E, Hamed A, Helal G, Baxi MD, Cerutis DR, Lassi NK. Neurotrophins and their receptors in nerve injury and repair. Neurochem Int 1997;30:347-374. (Pubitemid 27136016)
51. Forssmann U, Uguccioni M, Loetscher P, Dahinden CA, Langen H, Thelen M, Baggiolini M. Eotaxin-2, a novel CC chemokine that is selective for the chemokine receptor CCR3, and acts like eotaxin on human eosinophil and basophil leukocytes. J Exp Med 1997;185:2171-2176. (Pubitemid 27266000)
52. Gorio A, Lesma E, Madaschi L, Di Giulio AM. Co-administration of IGF-I and glycosaminoglycans greatly delays motor neurone disease and affects IGF-I expression in the wobbler mouse: A long-term study. J Neurochem 2002;81:194-202. (Pubitemid 34808867)
53. Hui KS. Brain-specific aminopeptidase: From enkephalinase to protector against neurodegeneration. Neurochem Res 2007;32:2062-2071.
54. Intapan PM, Niwattayakul K, Sawanyawisuth K, Chotmongkol V, Maleewong W. Cerebrospinal fluid eotaxin and eotaxin-2 levels in human eosinophilic meningitis associated with angiostrongyliasis. Cytokine. 2007;39:138-141. (Pubitemid 47513837)
55. Kato M, Yoshimura S, Kokuzawa J, Kitajima H, Kaku Y, Iwama T, Sinoda J, Kunisada T, Sakai N. Hepatocyte growth factor promotes neuronal differentiation of neural stem cells derived from embryonic stem cells. Neuroreport 2004;15:5-8. (Pubitemid 41614962)
56. Kim CH, Pelus LM, White JR, Broxmeyer HE. Macrophageinflammatory protein-3 beta/EBI1-ligand chemokine/CK beta-11, a CC chemokine, is a chemoattractant with a specificity for macrophage progenitors among myeloid progenitor cells. J Immunol 1998;161:2580-2585. (Pubitemid 28397077)
57. Kosaka N, Kodama M, Sasaki H, Yamamoto Y, Takeshita F, Takahama Y, Sakamoto H, Kato T, Terada M, Ochiya T. FGF-4 regulates neural progenitor cell proliferation and neuronal differentiation. FASEB J 2006;20:1484-1485.
58. Kust BM, Copray JC, Brouwer N, Troost D, Boddeke HW. Elevated levels of neurotrophins in human biceps brachii tissue of amyotrophic lateral sclerosis. Exp Neurol 2002;177:419-427. (Pubitemid 35366131)
59. Lapointe NP, Ung RV, Guertin PA. Plasticity in sublesionally located neurons following spinal cord injury. J Neurophysiol 2007;98:2497-2500. (Pubitemid 350127914)
60. Lykissas MG, Batistatou AK, Charalabopoulos KA, Beris AE. The role of neurotrophins in axonal growth, guidance, and regeneration. Curr Neurovasc Res 2007;4:143-151. (Pubitemid 46708904)
61. Martin TA, Jiang WG. Hepatocyte growth factor and its receptor signalling complex as targets in cancer therapy. Anticancer Agents Med Chem 2010;10:2-6.
62. Ochs G, Penn RD, York M, et al. A phase I/II trial of recombinant methionyl human brain derived neurotrophic factor administered by intrathecal infusion to patients with amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 2000;1:201-206.
63. Pang Y, Cai Z, Rhodes PG. Analysis of genes differentially expressed in astrocytes stimulated with lipopolysaccharide using cDNA arrays. Brain Res 2001;914:15-22. (Pubitemid 32905427)
64. Rajan AJ, Asensio VC, Campbell IL, Brosnan CF. Experimental autoimmune encephalomyelitis on the SJL mouse: Effect of gamma delta T cell depletion on chemokine and chemokine receptor expression in the central nervous system. J Immunol 2000;164:2120-2130. (Pubitemid 30108771)
65. Shih CH, van Eeden SF, Goto Y, Hogg JC. CCL23/myeloid progenitor inhibitory factor-1 inhibits production and release of polymorphonuclear leukocytes and monocytes from the bone marrow. Exp Hematol 2005;33:1101-1108. (Pubitemid 41416958)
66. Song R, Liu S, Leong KW. Effects of MIP-1 alpha, MIP-3 alpha, and MIP-3 beta on the induction of HIV Gag-specific immune response with DNA vaccines. Mol Ther 2007;15: 1007-1015. (Pubitemid 46621660)
67. Thoenen H. Neurotrophins and neuronal plasticity. Science 1995;270:593-598.
68. Tsuzaka K, Ishiyama T, Pioro EP, Mitsumoto H. Role of brain-derived neurotrophic factor in wobbler mouse motor neuron disease. Muscle Nerve 2001;24:474-480. (Pubitemid 32246782)
69. Walz A, Zwahlen R, Baggiolini M. Formation and biological properties of neutrophil activating peptide 2 (NAP-2). Adv Exp Med Biol 1991;305:39-46.
70. Waterhouse EG, Xu B. New insights into the role of brainderived neurotrophic factor in synaptic plasticity. Mol Cell Neurosci 2009;42:81-89.
71. Wilczak N, Kuhl N, Chesik D, Geerts A, Luiten P, De Keyser J. Insulin-like growth factor (IGF)-I binding to a cell membrane associated IGF binding protein-3 acid-labile subunit complex in human anterior pituitary gland. J Neurochem 2002;82:430-438. (Pubitemid 34774634)