Analysis of dosing regimen and reproducibility of intraspinal grafting of human spinal stem cells in immunosuppressed minipigs

Cell Transplantation

Volumn 19, Issue 9, 2010, Pages 1103-1122

  Usvald, Dusan ^a   Vodicka, Peter ^a   Hlucilova, Jana ^a   Prochazka, Radek ^a   Motlik, Jan ^a   Kuchorova, Karolina ^c,d   Johe, Karl ^b   Marsala, Silvia ^c   Scadeng, Miriam ^e   Kakinohana, Osamu ^c   Navarro, Roman ^c   Santa, Marian ^f   Hefferan, Michael P ^c   Yaksh, Tony L ^c   Marsala, Martin ^c,d  

^a INSTITUTE OF ANIMAL PHYSIOLOGY AND GENETICS   (Czech Republic)

^b Neuralstem Inc   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d INSTITUTE OF CHEMISTRY   (Slovakia)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF PRE OV   (Slovakia)

Author keywords

Dose response; Grafting; Immunosuppression; Spinal cord; Spinal stem cell; Survival

Indexed keywords

ANTIBODY; BROXURIDINE; TACROLIMUS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATAXIA; AUTOPSY; CELL DIFFERENTIATION; CELL SURVIVAL; CELL TRANSPLANTATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG BLOOD LEVEL; GRAFT REJECTION; HUMAN; HUMAN CELL; HUMAN SPINAL STEM CELL; HUMAN TISSUE; IMMUNE DEFICIENCY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTRASPINAL GRAFTING; JUGULAR VEIN; LUMBAR SPINAL CORD; MINIPIG; MOBILIZATION; MOTOR DYSFUNCTION; NEUROLOGIC EXAMINATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; REPRODUCIBILITY; SAFETY; SENSORIMOTOR FUNCTION; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL CORD VENTRAL HORN; STEM CELL; STEREOLOGY; VEIN CATHETERIZATION;

ANIMALS; CELL GROWTH PROCESSES; CELL SURVIVAL; FEMALE; GRAFT SURVIVAL; HUMANS; IMMUNOSUPPRESSION; MALE; MICE; NEURAL STEM CELLS; REPRODUCIBILITY OF RESULTS; SPINAL CORD; STEM CELL TRANSPLANTATION; SWINE; SWINE, MINIATURE;

ANIMALIA; RATTUS;

EID: 78649831388     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368910X503406     Document Type: Article

References (52)

1. Akesson, E.; Sandelin, M.; Kanaykina, N.; Aldskogius, H.; Kozlova, E. N. Long-term survival, robust neuronal differentiation, and extensive migration of human forebrain stem/progenitor cells transplanted to the adult rat dorsal root ganglion cavity. Cell Transplant. 17(10-11): 1115-1123; 2008.
2. Alexanian, A. R.; Crowe, M. J.; Kurpad, S. N. Efficient differentiation and integration of lineage-restricted neural precursors in the traumatically injured adult cat spinal cord. J. Neurosci. Methods 150(1):41-46; 2006.
3. Anderson, D. K.; Howland, D. R.; Reier, P. J. Fetal neural grafts and repair of the injured spinal cord. Brain Pathol. 5(4):451-457; 1995.
4. Barratt, D. M.; Van Meter, K. Decompression sickness in Miskito Indian lobster divers: Review of 229 cases. Aviat. Space Environ. Med. 75(4):350-353; 2004.
5. Bjugn, R. The use of the optical disector to estimate the number of neurons, glial and endothelial cells in the spinal cord of the mouse - with a comparative note on the rat spinal cord. Brain Res. 627(1):25-33; 1993.
6. Bjugn, R.; Gundersen, H. J. Estimate of the total number of neurons and glial and endothelial cells in the rat spinal cord by means of the optical disector. J. Comp. Neurol. 328(3):406-414; 1993.
7. Casas, C. E.; Guest, J. D. Percutaneous endoscopic cellular transplantation into the lower lumbar spinal cord. Neurosurgery 54(4):950-955; 2004.
8. Cizkova, D.; Kakinohana, O.; Kucharova, K.; Marsala, S.; Johe, K.; Hazel, T.; Hefferan, M. P.; Marsala, M. Functional recovery in rats with ischemic paraplegia after spinal grafting of human spinal stem cells. Neuroscience 147(2):546-560; 2007.
9. Couillard-Despres, S.; Winner, B.; Schaubeck, S.; Aigner, R.; Vroemen, M.; Weidner, N.; Bogdahn, U.; Winkler, J.; Kuhn, H. G.; Aigner, L. Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 21(1): 1-14; 2005.
10. Cummings, B. J.; Uchida, N.; Tamaki, S. J.; Salazar, D. L.; Hooshmand, M.; Summers, R.; Gage, F. H.; Ander- son, A. J. Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc. Natl. Acad. Sci. USA 102(39):14069-14074; 2005.
11. Feron, F.; Perry, C.; Cochrane, J.; Licina, P.; Nowitzke, A.; Urquhart, S.; Geraghty, T.; Mackay-Sim, A. Autologous olfactory ensheathing cell transplantation in human spinal cord injury. Brain 128(Pt. 12):2951-2960; 2005.
12. Gleeson, J. G.; Lin, P. T.; Flanagan, L. A.; Walsh, C. A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23(2): 257-271; 1999.
13. Hefferan, M. P.; Kakinohana, O.; Johe, K.; Marsala, M. Long term survival of human neural stem cells after spinal tranansplantation in nude rats. 13th ASNTR Annual Meeting, Clearwater, FL; A28; 2007.
14. Howland, D. S.; Liu, J.; She, Y.; Goad, B.; Maragakis, N. J.; Kim, B.; Erickson, J.; Kulik, J.; DeVito, L.; Psaltis, G.; DeGennaro, L. J.; Cleveland, D. W.; Rothstein, J. D. Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc. Natl. Acad. Sci. USA 99(3): 1604-1609; 2002.
15. Jendelova, P.; Herynek, V.; Urdzikova, L.; Glogarova, K.; Kroupova, J.; Andersson, B.; Bryja, V.; Burian, M.; Hajek, M.; Sykova, E. Magnetic resonance tracking of transplanted bone marrow and embryonic stem cells labeled by iron oxide nanoparticles in rat brain and spinal cord. J. Neurosci. Res. 76(2):232-243; 2004.
16. Johe, K. K.; Hazel, T. G.; Muller, T.; Dugich-Djordjevic, M. M.; McKay, R. D. Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev. 10(24):3129-3140; 1996.
17. Kakinohana, O.; Hefferan, M. P.; Nakamura, S.; Kakinohana, M.; Galik, J.; Tomori, Z.; Marsala, J.; Yaksh, T. L.; Marsala, M. Development of gaba-sensitive spasticity and rigidity in rats after transient spinal cord ischemia: A qualitative and quantitative electrophysiological and histopathological study. Neuroscience 141(3):1569-1583; 2006.
18. Kao, C. C.; Shimizu, Y.; Perkins, L. C.; Freeman, L. W. Experimental use of cultured cerebellar cortical tissue to inhibit the collagenous scar following spinal cord transection. J. Neurosurg. 33(2):127-139; 1970.
19. Kohama, I.; Lankford, K. L.; Preiningerova, J.; White, F. A.; Vollmer, T. L.; Kocsis, J. D. Transplantation of cryopreserved adult human Schwann cells enhances axonal conduction in demyelinated spinal cord. J. Neurosci. 21(3):944-950; 2001.
20. Lazorthes, Y.; Sallerin-Caute, B.; Verdie, J. C.; Bastide, R.; Carillo, J. P. Chronic intrathecal baclofen administration for control of severe spasticity. J. Neurosurg. 72(3): 393-402; 1990.
21. Lepore, A. C.; Bakshi, A.; Swanger, S. A.; Rao, M. S.; Fischer, I. Neural precursor cells can be delivered into the injured cervical spinal cord by intrathecal injection at the lumbar cord. Brain Res. 1045(1-2):206-216; 2005.
22. Lepore, A. C.; Fischer, I. Lineage-restricted neural precursors survive, migrate, and differentiate following transplantation into the injured adult spinal cord. Exp. Neurol. 194(1):230-242; 2005.
23. Liu, Y.; Kim, D.; Himes, B. T.; Chow, S. Y.; Schallert, T.; Murray, M.; Tessler, A.; Fischer, I. Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospinal axons and recovery of forelimb function. J. Neurosci. 19(11):4370-4387; 1999.
24. Marangos, P. J.; Schmechel, D. E.; Parma, A. M.; Goodwin, F. K. Developmental profile of neuron-specific (NSE) and non-neuronal (NNE) enolase. Brain Res. 190(1):185-193; 1980.
25. Marsala, J.; Sulla, I.; Santa, M.; Marsala, M.; Zacharias, L.; Radonak, J. Mapping of the canine lumbosacral spinal cord neurons by Nauta method at the end of the early phase of paraplegia induced by ischemia and reperfusion. Neuroscience 45(2):479-494; 1991.
26. Marsala, M.; Hefferan, M. P.; Kakinohana, O.; Nakamura, S.; Marsala, J.; Tomori, Z. Measurement of peripheral muscle resistance in rats with chronic ischemia-induced paraplegia or morphine-induced rigidity using a semi-automated computer-controlled muscle resistance meter. J. Neurotrauma 22(11):1348-1361; 2005.
27. Marsala, M.; Kakinohana, O.; Yaksh, T. L.; Tomori, Z.; Marsala, S.; Cizkova, D. Spinal implantation of hNT neurons and neuronal precursors: Graft survival and functional effects in rats with ischemic spastic paraplegia. Eur. J. Neurosci. 20(9):2401-2414; 2004.
28. Matsushita, A.; Smith, C. M. Spinal cord function in postischemic rigidity in the rat. Brain Res. 19(3):395-410; 1970.
29. McDonald, J. W.; Liu, X. Z.; Qu, Y.; Liu, S.; Mickey, S. K.; Turetsky, D.; Gottlieb, D. I.; Choi, D. W. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat. Med. 5(12):1410-1412; 1999.
30. Mitsui, T.; Shumsky, J. S.; Lepore, A. C.; Murray, M.; Fischer, I. Transplantation of neuronal and glial restricted precursors into contused spinal cord improves bladder and motor functions, decreases thermal hypersensitivity, and modifies intraspinal circuitry. J. Neurosci. 25(42):9624-9636; 2005.
31. Mothe, A. J.; Kulbatski, I.; Parr, A.; Mohareb, M.; Tator, C. H. Adult spinal cord stem/progenitor cells transplanted as neurospheres preferentially differentiate into oligodendrocytes in the adult rat spinal cord. Cell Transplant. 17(7):735-751; 2008.
32. Muotri, A. R.; Nakashima, K.; Toni, N.; Sandler, V. M.; Gage, F. H. Development of functional human embryonic stem cell-derived neurons in mouse brain. Proc. Natl. Acad. Sci. USA 102(51):18644-18648; 2005.
33. Radtke, C.; Akiyama, Y.; Brokaw, J.; Lankford, K. L.; Wewetzer, K.; Fodor, W. L.; Kocsis, J. D. Remyelination of the nonhuman primate spinal cord by transplantation of H-transferase transgenic adult pig olfactory ensheathing cells. FASEB J. 18(2):335-337; 2004.
34. Reier, P. J.; Bregman, B. S.; Wujek, J. R. Intraspinal transplantation of embryonic spinal cord tissue in adult and neonatal rats: Evidence for topographical differentiation and axonal interactions with the host CNS. In: Bjorklund, A.; Stenevi, U., eds. Neural grafting in the mammalian CNS. Amsterdam: Elsevier; 1985:257-263.
35. Reier, P. J.; Bregman, B. S.; Wujek, J. R. Intraspinal transplantation of embryonic spinal cord tissue in neonatal and adult rats. J. Comp. Neurol. 247(3):275-296; 1986.
36. Reier, P. J.; Stokes, B. T.; Thompson, F. J.; Anderson, D. K. Fetal cell grafts into resection and contusion/compression injuries of the rat and cat spinal cord. Exp. Neurol. 115(1):177-188; 1992.
37. Sugimoto, T.; Bennett, G. J.; Kajander, K. C. Transsynaptic degeneration in the superficial dorsal horn after sciatic nerve injury: Effects of a chronic constriction injury, transection, and strychnine. Pain 42(2):205-213; 1990.
38. Sun, C. N.; Araoz, C.; Lucas, G.; Morgan, P. N.; White, H. J. Amyotrophic lateral sclerosis. Inclusion bodies in a case of the classic sporadic form. Ann. Clin. Lab. Sci. 5(1):38-44; 1975.
39. Taira, Y.; Marsala, M. Effect of proximal arterial perfusion pressure on function, spinal cord blood flow, and histopathologic changes after increasing intervals of aortic occlusion in the rat. Stroke 27(10):1850-1858; 1996.
40. Tarlov, I. M. Rigidity in man due to spinal interneuron loss. Arch. Neurol. 16(5):536-543; 1967.
41. Totoiu, M. O.; Nistor, G. I.; Lane, T. E.; Keirstead, H. S. Remyelination, axonal sparing, and locomotor recovery following transplantation of glial-committed progenitor cells into the MHV model of multiple sclerosis. Exp. Neurol. 187(2):254-265; 2004.
42. Tuszynski, M. H.; Grill, R.; Jones, L. L.; McKay, H. M.; Blesch, A. Spontaneous and augmented growth of axons in the primate spinal cord: Effects of local injury and nerve growth factor-secreting cell grafts. J. Comp. Neurol. 449(1):88-101; 2002.
43. Urdzikova, L.; Jendelova, P.; Glogarova, K.; Burian, M.; Hajek, M.; Sykova, E. Transplantation of bone marrow stem cells as well as mobilization by granulocyte-colony stimulating factor promotes recovery after spinal cord injury in rats. J. Neurotrauma 23(9):1379-1391; 2006.
44. Van Harreveld, A.; Marmont, G. The course of recovery of the spinal cord from asphyxia. J. Neurophysiol. 2:101-111; 1939.
45. West, M. J.; Slomianka, L.; Gundersen, H. J. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231(4):482-497; 1991.
46. Willing, A. E.; Garbuzova-Davis, S.; Saporta, S.; Milliken, M.; Cahill, D. W.; Sanberg, P. R. hNT neurons delay onset of motor deficits in a model of amyotrophic lateral sclerosis. Brain Res. Bull. 56(6):525-530; 2001.
47. Wolf, H. K.; Crain, B. J.; Siddique, T. Degeneration of the substantia nigra in familial amyotrophic lateral sclerosis. Clin. Neuropathol. 10(6):291-296; 1991.
48. Wrathall, J. R.; Rigamonti, D. D.; Braford, M. R.; Kao, C. C. Reconstruction of the contused cat spinal cord by the delayed nerve graft technique and cultured peripheral non-neuronal cells. Acta Neuropathol. (Berl.). 57(1):59-69; 1982.
49. Xu, L.; Yan, J.; Chen, D.; Welsh, A. M.; Hazel, T.; Johe, K.; Hatfield, G.; Koliatsos, V. E. Human neural stem cell grafts ameliorate motor neuron disease in SOD-1 transgenic rats. Transplantation 82(7):865-875; 2006.
50. Yan, J.; Xu, L.; Welsh, A. M.; Hatfield, G.; Hazel, T.; Johe, K.; Koliatsos, V. E. Extensive neuronal differentiation of human neural stem cell grafts in adult rat spinal cord. PLoS Med. 4(2):e39; 2007.
51. Yoshiyama, M.; Asamoto, S.; Kobayashi, N.; Sugiyama, H.; Doi, H.; Sakagawa, H.; Ida, M. Spinal cord decompression sickness associated with scuba diving: Correlation of immediate and delayed magnetic resonance imaging findings with severity of neurologic impairment - a report on 3 cases. Surg. Neurol. 67(3):283-287; 2007.
52. Zhang, L.; Gu, S.; Zhao, C.; Wen, T. Combined treatment of neurotrophin-3 gene and neural stem cells is propitious to functional recovery after spinal cord injury. Cell Transplant. 16(5):475-481; 2007.