Transplantation of human adipose tissue-derived stem cells delays clinical onset and prolongs life span in ALS mouse model

Cell Transplantation

Volumn 23, Issue 12, 2014, Pages 1585-1597

  Kim, Kwang S ^a   Lee, Hong J ^a,b   An, Jin ^a   Kim, Yun B ^c   Ra, Jung Chan ^d   Lim, Inja ^a   Kim, Seung U ^a,b  

^a Chung Ang University College of Medicine   (South Korea)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c Chungbuk National University   (South Korea)

^d K STEMCELL Co Ltd   (South Korea)

Author keywords

Adipose tissue derived stem cells (ASCs); Amyotrophic lateral sclerosis (ALS); Cell therapy; Cu Zn superoxide dismutase (SOD1); Cytokines; Mesenchymal stem cells (MSCs); Neuroprotection; Neurotrophic factor; Transgenic mouse; Transplantation

Indexed keywords

CYTOKINE; HYDROGEN PEROXIDE; NEUROPROTECTIVE AGENT;

ADIPOSE TISSUE; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL; ANIMAL BEHAVIOR; CELL DIFFERENTIATION; CELL SURVIVAL; CYTOLOGY; DISEASE MODEL; DONOR; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; INTRAVENOUS DRUG ADMINISTRATION; LONGEVITY; MALE; METABOLISM; MIDDLE AGED; MOTOR ACTIVITY; MOUSE; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; SECRETION (PROCESS); SPINAL CORD; STEM CELL; STEM CELL TRANSPLANTATION; VERY ELDERLY;

ADIPOSE TISSUE; AGED; AGED, 80 AND OVER; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BEHAVIOR, ANIMAL; CELL DIFFERENTIATION; CELL SURVIVAL; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; HYDROGEN PEROXIDE; INJECTIONS, INTRAVENOUS; INJECTIONS, INTRAVENTRICULAR; LONGEVITY; MALE; MICE; MIDDLE AGED; MOTOR ACTIVITY; NEURONS; NEUROPROTECTIVE AGENTS; SPINAL CORD; STEM CELL TRANSPLANTATION; STEM CELLS; TISSUE DONORS;

EID: 84920096082     PISSN: 09636897     EISSN: 15553892     Source Type: Journal    
DOI: 10.3727/096368913X673450     Document Type: Article

References (44)

1. Aguado, B. A.; Mulyasasmita, W.; Su, J.; Lampe, K. J.; Heilshorn, S. C. Improving viability of stem cells during syringe needle flow through the design of hydrogel cell carriers. Tissue Eng. 18:806-815; 2012.
2. Boillee, S.; Van de Velde, C.; Cleveland, D. W. ALS: A disease of motor neurons and their nonneuronal neighbors. Neuron 52:39-59; 2008.
3. Chu, K.; Kim, M.; Jeong, S. W.; Kim, S. U.; Yoon, B. W. Human neural stem cells can migrate, differentiate and integrate after intravenous transplantation in adult rats with transient forebrain ischemia. Neurosci. Lett. 343: 637-643; 2003.
4. Cleveland, D. W.; Rothstein, J. D. From Charcot to Lou Gehrig: Deciphering selective motor neuron death in ALS. Nat. Rev. Neurosci. 2:806-819; 2001.
5. Constantin, G.; Marconi, S.; Rossi, B.; Angiari, S.; Calderan, L.; Anghileri, E.; Gini, B.; Bach, S. D.; Martinello, M.; Bifari, F.; Galie, M.; Turano, E.; Budui, S.; Sbarbati, A.; Krampera, M.; Bonetti, B. Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells 27:2624-2635; 2009.
6. Dimos, J. T.; Rodolfa, K. T.; Niakan, K. K.; Weisenthal, L. M.; Mitsumoto, H.; Chung, W.; Croft, G. F.; Saphier, G.; Leibel, R.; Goland, R.; Wichterle, H.; Henderson, C. E.; Eggan, K. Induced pluripotent stem cells generated from patient with ALS can be differentiated into motor neurons. Science 321:1218-1221; 2008.
7. Draqunow, M.; MacGibbon, G. A.; Lawlor, P.; Butterworth, N.; Connor, B. Apoptosis, neurotrophic factors and neurodegeneration. Rev. Neurosci. 8:223-265; 1997.
8. Erba, P.; Terenghi, G.; Kingham, P. J. Neural differentiation and therapeutic potential of adipose tissue derived stem cells. Curr. Stem Cell Res. Ther. 5:153-160; 2010.
9. Ferrero, I.; Mazzini, L.; Rustichelli, D.; Gunetti, M.; Mareschi, K. Bone marrow mesenchymal stem cells from healthy donors and sporadic amyotrophic lateral sclerosis patients. Cell Transplant. 17:255-266; 2008.
10. Flax, J. D.; Aurora, S.; Yang, C.; Simonin, C.; Wills, A. M.; Billinghurst, L.; Jendoubi, M.; Sidman, R. L.; Wolfe, J. H.; Kim, S. U.; Snyder, E. Y. Engraftable human neural stem cells respond to developmental cues, replace neurons and express foreign genes. Nat. Biotechnol. 16:1033-1039; 1998.
11. Gimble, J. M.; Katz, A. J.; Bunnell, B. A. Adipose-derived stem cells for regenerative medicine. Circ. Res. 100: 1249-1260; 2007.
12. Goldman, S. Stem and progenitor cell-based therapy of the human central nervous system. Nat. Biotechnol. 7:862- 871; 2004.
13. Gurney, M. E.; Pu, H.; Chiu, A. Y.; Dal Canto, M. C.; Polchow, C. Y.; Alexander, D. D.; Caliendo, J.; Hentati, A.; Kwon, Y. W.; Deng, H. X. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264:1772-1775; 1994.
14. Harper, J. M.; Krishnan, C.; Darman, J. S. Axonal growth of embryonic stem cell derived motoneurons in vitro and in motoneuron-injured adult rats. Proc. Natl. Acad. Sci. USA 101:7123-7128; 2004.
15. Hefferan, M. P.; Galik, J.; Kakinohana, O.; Sekerkova, G.; Santucci, C.; Marsala, S.; Navarro, R.; Hruska-Plochan, M.; Johe, K.; Feldman, E.; Cleveland, D. W.; Marsala, M. Human neural stem cell replacement therapy for amyotrophic lateral sclerosis by spinal transplantation. PLoS One 7:e42614; 2012.
16. Hwang, D. H.; Lee, H. J.; Park, I. H.; Seok, J. I.; Kim, B. G.; Joo, I. S.; Kim, S. U. Intrathecal transplantation of human neural stem cells overexpressing VEGF provide behavioral improvement, disease onset delay and survival extension in transgenic ALS mice. Gene Ther. 16:1234- 1244; 2009.
17. Kaal, E. C.; Veldman, H.; Sodaar, P.; Joosten, E.; DopBar, P. R. Oxidant treatment causes a dose-dependent phenotype of apoptosis in cultured motoneurons. J. Neurosci. Res. 54: 778-786; 1998.
18. Kaspar, B.; Llado, J.; Sherkat, N.; Rothstein, J. D.; Gage, F. H. Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science 301:839-842; 2003.
19. Kerr, D. A.; Lladó, J.; Shamblott, M. J.; Maragakis, N. J.; Irani, D. N.; Crawford, T. O.; Krishnan, C.; Dike, S.; Gearhart, J. D.; Rothstein, J. D. Human embryonic germ cell derivatives facilitate motor recovery of rats with diffuse motor neuron injury. J. Neurosci. 23:5131-5140; 2003.
20. Kim, J. M.; Lee, S. T.; Chu, K.; Jung, K. H.; Song, E. C.; Kim, S. J.; Sinn, D. I.; Kim, J. H.; Park, D. K.; Kang, K. M.; Hong, N.; Park, H. K.; Won, C. H.; Kim, K. H.; Kim, M.; Lee, S.; Roh, J. K. Systemic transplantation of human adipose stem cells attenuated cerebral inflammation and degeneration in a hemorrhagic stroke model. Brain Res. 1183:43-50; 2007.
21. Kim, K. S.; Lee, H. J.; Jeong, H. S.; Li, J.; Teng, Y. D.; Sidman, R. L.; Snyder, E. Y.; Kim, S. U. Self-renewal induced efficiently, safely, and effective therapeutically with one regulatable gene in a human somatic progenitor cell. Proc. Natl. Acad. Sci. USA 108:4876-4881; 2011.
22. Kim, S. U. Human neural stem cells genetically modified for brain repair in neurological disorders. Neuropathology 24:159-174; 2000.
23. Kim, S. U.; de Vellis, J. Stem cell-based cell therapy in neurological diseases: A review. J. Neurosci. Res. 87: 2183-2200; 2009.
24. Kim, S. U.; Krieger, C.; Eisen, A. Human and rodent spinal cord neurons in culture. Adv. Neurol. 56:57-66; 1991.
25. Kim, S. U.; Lee, H. J.; Kim, Y. B. Neural stem cell-based treatment for neurodegenerative diseases. Neuropathology 33:491-504; 2013.
26. Lee, S. T.; Chu, K.; Jung, K. H.; Kim, S. J.; Kim, D. H.; Kim, S. U.; Roh, J. K. Antiinflammatory mechanism of intravascular neural stem cell transplantation in hemorrhagic stroke. Brain 131:616-629; 2008.
27. Lindvall, O.; Kokaia, Z.; Martinez-Serrano, A. Stem cell therapy for human neurodegenerative disorders-How to make it work. Nat. Med. 10(suppl):S42-S50; 2004.
28. Liu, D.; Wen, J.; Liu, J.; Li, L. The roles of free radicals in amyotrophic lateral sclerosis: Reactive oxygen species and elevated oxidation of protein, DNA, and membrane phospholipids. FASEB J. 13:2318-2328; 1999.
29. Mazzini, L.; Mareschi, K.; Ferrero, I.; Miglioretti, M.; Stecco, A. Mesenchymal stromal cell transplantation in amyotrophic lateral sclerosis: A long-term safety study. Cytotherapy 14:56-60; 2012.
30. Miles, G. B.; Yohn, D. C.; Wichterle, H. Functional properties of motoneurons derived from mouse embryonic stem cells. J. Neurosci. 24:7848-7858; 2004.
31. Mitrecic, D.; Nicaise, C.; Gajovic, S.; Pochet, R. Distribution, differentiation, and survival of intravenously administered neural stem cells in a rat model of amyotrophic lateral sclerosis. Cell Transplant. 19:537-548; 2010.
32. Nayak, M. S.; Kim, Y. S.; Goldman, M.; Keirstead, H. S.; Kerr, D. A. Cellular therapies in motor neuron diseases. Biochim. Biophys. Acta 1762:1128-1138; 2006.
33. Puissant, B.; Barreau, C.; Bourin, P.; Clavel, C.; Corre, J. Immunomodulatory effect of human adipose tissue-derived adult stem cells: Comparison with bone marrow mesenchymal stem cells. Br. J. Haematol. 129:118-129; 2005.
34. Ra, J. C.; Shin, I. S.; Kim, S. H.; Kang, S.; Yoon, E. J. Safety of intravenous infusion of human adipose tissuederived mesenchymal stem cells in animals and humans. Stem Cells Dev. 20:1297-1308; 2011.
35. Rehman, J.; Traktuev, D.; Li, J.; Merfeld-Clauss, S.; Temm-Grove, C. J; Bovenkerk, J. E.; Pell, C. L.; Johnstone, B. H.; Considine, R. V.; March, K. L. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 109:1292-1298; 2004.
36. Riley, J.; Federici, T.; Polak, M.; Kelly, C.; Glass, J.; Raore, B.; Taub, J.; Kesner, V.; Feldman, E. L.; Boulis, N. M. Intraspinal stem cell transplantation in amyotrophic lateral sclerosis: A phase I safety trial, technical note, and lumbar safety outcomes. Neurosurgery 71:405-416; 2012.
37. Rowland, L. P.; Shneider, N. A. Amyotrophic lateral sclerosis. N. Engl. J. Med. 344:1688-1700; 2001.
38. Salgado, A. J.; Reis, R. L.; Sousa, N. J.; Gimble, J. M. Adipose tissue derived stem cells secretome: Soluble factors and their roles in regenerative medicine. Curr. Stem Cell Res. Ther. 5:103-110; 2010.
39. Schäffler, A.; Büchler, C. Adipose tissue-derived stromal cells-basic and clinical implications for novel cell-based therapies. Stem Cells 25:818-827; 2007.
40. Song, S. Y.; Chung, H. M.; Sung, J. H. The pivotal role of VEGF in adipose derived-stem-cell-mediated regeneration. Expert Opin. Biol. Ther. 10:1529-1537; 2010.
41. Wei, X.; Du, Z.; Zhao, L.; Feng, D.; Wei, G.; He, Y.; Tan, J.; Lee, W. H.; Hampel, H.; Dodel, R.; Johnstone, B. H.; March, K. L.; Farlow, M. R.; Du, Y. The conditioned media of adipose stromal cells protect against hypoxia-ischemia induced brain damage in neonatal rats. Stem Cells 27: 478-488; 2009.
42. West, M. J.; Slomianka, L.; Gundersen, H. J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionators. Anat. Rec. 231:482-497; 1991.
43. Wichterle, H.; Lieberam, I.; Porter, J. A.; Jessell, T. M. Directed differentiation of embryonic stem cells into motor neurons. Cell 110:385-397; 2002.
44. Zuk, P. A.; Zhu, M.; Ashjian, P.; De Ugarte, D. A.; Huang, J. I. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell 13:4279-4295; 2002.