A comparison of the behavioral and anatomical outcomes in sub-acute and chronic spinal cord injury models following treatment with human mesenchymal precursor cell transplantation and recombinant decorin

Experimental Neurology

Volumn 248, Issue , 2013, Pages 343-359

  Hodgetts, Stuart I ^a   Simmons, Paul J ^c,d   Plant, Giles W ^a,b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^d Mesoblast Limited   (Australia)

Author keywords

Cellular therapy; Chronic; Contusion; Decorin; Mesenchymal precursors; Proteoglycan; Spinal cord; Sub acute; Transplantation

Indexed keywords

DECORIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIORAL SCIENCE; CELL SURVIVAL; COCULTURE; COMPARATIVE STUDY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; FUNCTIONAL ASSESSMENT; GLIA CELL; GRAFT SURVIVAL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL TRANSPLANTATION; NERVE FIBER GROWTH; NEUROANATOMY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD INJURY;

CELLULAR THERAPY; CHRONIC; CONTUSION; DECORIN; MESENCHYMAL PRECURSORS; PROTEOGLYCAN; SPINAL CORD; SUB-ACUTE; TRANSPLANTATION;

ANIMALS; AXONS; COCULTURE TECHNIQUES; COMBINED MODALITY THERAPY; DECORIN; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MOTOR ACTIVITY; NERVE REGENERATION; NEURITES; RATS; RATS, NUDE; RECOMBINANT PROTEINS; RECOVERY OF FUNCTION; SPINAL CORD; SPINAL CORD INJURIES; TREATMENT OUTCOME;

EID: 84881096419     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.06.018     Document Type: Article

References (74)

1. Aggarwal S., Pettinger M.F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005, 105:1815-1822.
2. Al Haj Zen A., Lafont A., Durand E., Brasselet C., Lemarchand P., Godeau G., Gogly B. Effect of adenovirus-mediated overexpression of decorin on metalloproteinases, tissue inhibitors of metalloproteinases and cytokines secretion by human gingival fibroblasts. Matrix Biol. 2003, 22(3):251-258. (May).
3. Bakshi A., Barshinger A.L., Swanger S.A., Madhavani V., Shumsky J.S., Neuhuber B., Fischer I. Lumbar puncture delivery of bone marrow stromal cells in spinal cord contusion: a novel method for minimally invasive cell transplantation. J. Neurotrauma 2006, 23:55-65.
4. Barkho B.Z., Song H., Aimone J.B., Smrt R.D., Kuwabara T., Nakashima K., Gage F.H., Zhao X. Identification of astrocyte-expressed factors that modulate neural stem/progenitor cell differentiation. Stem Cells Dev. 2006, 15(3):407-421.
5. Basso D.M., Beattie M.S., Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 1995, 12:1-21.
6. Beck K.D., Nguyen H.X., Galvan M.D., Salazar D.L., Woodruff T.M., Anderson A.J. Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain 2010, 133:433-447.
7. Brachmann R., Lindquist P.B., Nagashima M., Kohr W., Lipari T., Napier M., Derynck R. Transmembrane TGF-alpha precursors activate EGF\TGF-alpha receptors. Cell 1989, 56:691-700.
8. Braunewell K.H., Pesheva P., McCarthy J.B., Furcht L.T., Schmitz B., Schachner M. Functional involvement of sciatic nerve-derived versican- and decorin-like molecules and other chondroitin sulphate proteoglycans in ECM-mediated cell adhesion and neurite outgrowth. Eur. J. Neurosci. 1995, 7:805-814.
9. Caplan A.I. What's in a name?. Tissue Eng. A 2010, 16:2415-2417.
10. Chassoux D., Dokhelar M.C., Tursz T., Salomon J.C. Antibody-dependent cellular cytotoxicity and natural killing in nude rats: quantitative study according to age and sex. Ann. Immunol. (Paris) 1983, 134D:309-318.
11. Comalada M., Cardo M., Xaus J., Valledor A.F., Lloberas J., Ventura F., Celada A. Decorin reverses the repressive effect of autocrine-produced TGF-beta on mouse macrophage activation. J. Immunol. 2003, 170:4450-4456.
12. Davies S.J., Goucher D.R., Doller C., Silver J. Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J. Neurosci. 1999, 19:5810-5822.
13. Davies J.E., Tang X., Denning J.W., Archibald S.J., Davies S.J. Decorin suppresses neurocan, brevican, phosphacan and NG2 expression and promotes axon growth across adult rat spinal cord injuries. Eur. J. Neurosci. 2004, 19(5):1226-1242. (Mar).
14. Davies J.E., Tang X., Bournat J.C., Davies S.J. Decorin promotes plasminogen/plasmin expression within acute spinal cord injuries and by adult microglia in vitro. J. Neurotrauma 2006, 23:397-408.
15. de Haro J., Zurita M., Ayllón L., Vaquero J. Detection of 111In-oxine-labeled bone marrow stromal cells after intravenous or intralesional administration in chronic paraplegic rats. Neurosci. Lett. 2005, 377(1):7-11. (Mar 22) (Electronic publication ahead of print, 2004 Dec 15).
16. Deshmane S.L., Kremlev S., Amini S., Sawaya B.E. Monocyte chemoattractant protein-1 (MCP-1): an overview. J. Interferon Cytokine Res. 2009, 6:313-326.
17. Fawcett J.W., Curt A., Steeves J.D., Coleman W.P., Tuszynski M.H., Lammertse D., Bartlett P.F., Blight A.R., Dietz V., Ditunno J., Dobkin B.H., Havton L.A., Ellaway P.H., Fehlings M.G., Privat A., Grossman R., Guest J.D., Kleitman N., Nakamura M., Gaviria M., Short D. Guidelines for the conduct of clinical trials for spinal cord injury as developed by the ICCP panel: spontaneous recovery after spinal cord injury and statistical power needed for therapeutic clinical trials. Spinal Cord 2007, 45:190-205.
18. Fitch M.T., Silver J. CNS injury, glial scars, and inflammation: inhibitory extracellular matrices and regeneration failure. Exp. Neurol. 2008, 2:294-301.
19. Gensel J.C., Donnelly D.J., Popovich P.G. Spinal cord injury therapies in humans: an overview of current clinical trials and their potential effects on intrinsic CNS macrophages. Expert Opin. Ther. Targets 2011, 15:505-518.
20. Goldoni S., Owens R.T., McQuillan D.J., Shriver Z., Sasisekharan R., Birk D.E., Campbell S., Iozzo R.V. Biologically active decorin is a monomer in solution. J. Biol. Chem. 2004, 279:6606-6612.
21. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003, 3:23-35.
22. Gronthos S., Simmons P.J. The biology and application of human bone marrow stromal cell precursors. J. Hematother. 1996, 5:15-23.
23. Hermann A., Liebau S., Gastl R., Fickert S., Habisch H.J., Fiedler J., Schwarz J., Brenner R., Storch A. Comparative analysis of neuroectodermal differentiation capacity of human bone marrow stromal cells using various conversion protocols. J. Neurosci. Res. 2006, 83:1502-1514.
24. Hildebrand A., Romaris M., Rasmussen L.M., Heinegard D., Twardzik D.R., Border W.A., Ruoslahti E. Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor beta. Biochem. J. 1994, 302(Pt 2):527-534.
25. Hill C.E., Beattie M.S., Bresnahan J.C. Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp. Neurol. 2001, 171:153-169.
26. Himes B.T., Neuhuber B., Coleman C., Kushner R., Swanger S.A., Kopen G.C., Wagner J., Shumsky J.S., Fischer I. Recovery of function following grafting of human bone marrow-derived stromal cells into the injured spinal cord. Neurorehabil. Neural Repair 2006, 20:278-296.
27. Hocking A.M., Shinomura T., McQuillan D.J. Leucine-rich repeat glycoproteins of the extracellular matrix. Matrix Biol. 1998, 17:1-19.
28. Hodgetts S., Plant G.W., Harvey A. Spinal cord injury: experimental animal models and relation to human therapy. The Spinal Cord 2008, Elsevier, London. C. Watson, G. Paxinos, G. Kayalioglu (Eds.).
29. +) from spinal cord injury patients improve functional recovery and tissue sparing in an acute spinal cord injury rat model. Cell Transplant. 2013, 22:393-412.
30. Hofstetter C.P., Schwarz E.J., Hess D., Widenfalk J., El Manira A., Prockop D.J., Olson L. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:2199-2204.
31. Hou S.Y., Zhang H.Y., Quan D.P., Liu X.L., Zhu J.K. Tissue-engineered peripheral nerve grafting by differentiated bone marrow stromal cells. Neuroscience 2006, 140:101-110.
32. Iozzo R.V., Buraschi S., Genua M., Xu S.Q., Solomides C.C., Peiper S.C., Gomella L.G., Owens R.C., Morrione A. Decorin antagonizes IGF receptor I (IGF-IR) function by interfering with IGF-IR activity and attenuating downstream signaling. J. Biol. Chem. 2011, 286(40):34712-34721. (Oct. 7) (Electronic publication ahead of print, 2011 Aug 12). 10.1074/jbc.M111.262766.
33. Jain A., McKeon R.J., Brady-Kalnay S.M., Bellamkonda R.V. Sustained delivery of activated Rho GTPases and BDNF promotes axon growth in CSPG-rich regions following spinal cord injury. PLoS One 2011, 6:e16135.
34. Keene D.R., San Antonio J.D., Mayne R., McQuillan D.J., Sarris G., Santoro S.A., Iozzo R.V. Decorin binds near the C terminus of type I collagen. J. Biol. Chem. 2000, 275:21801-21804.
35. Kleitman N.W.P., Bunge R.P. Tissue culture methods for the study of myelination. Culturing Nerve Cells 1998, 545-594. 2nd ed. G.A. Banker, K. Goslin (Eds.).
36. Köninger J., Giese N.A., Bartel M., di Mola F.F., Berberat P.O., di Sebastiano P., Giese T., Büchler M.W., Friess H. The ECM proteoglycan decorin links desmoplasia and inflammation in chronic pancreatitis. J. Clin. Pathol. 2006, 59(1):21-27. (Jan).
37. Kopen G.C., Prockop D.J., Phinney D.G. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:10711-10716.
38. Kramer B.C., Woodbury D., Black I.B. Adult rat bone marrow stromal cells express genes associated with dopamine neurons. Biochem. Biophys. Res. Commun. 2006, 343:1045-1052.
39. Krumdieck R., Hook M., Rosenberg L.C., Volanakis J.E. The proteoglycan decorin binds C1q and inhibits the activity of the C1 complex. J. Immunol. 1992, 149:3695-3701.
40. Laremore T.N., Ly M., Zhang Z., Solakyildirim K., McCallum S.A., Owens R.T., Linhardt R.J. Domain structure elucidation of human decorin glycosaminoglycans. Biochem. J. 2010, 431:199-205.
41. Logan A., Baird A., Berry M. Decorin attenuates gliotic scar formation in the rat cerebral hemisphere. Exp. Neurol. 1999, 159:504-510.
42. Mauviel A., Santra M., Chen Y.Q., Uitto J., Iozzo R.V. Transcriptional regulation of decorin gene expression. Induction by quiescence and repression by tumor necrosis factor-alpha. J. Biol. Chem. 1995, 270:11692-11700.
43. Meirelles Lda S., Fontes A.M., Covas D.T., Caplan A.I. Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev. 2009, 20:419-427.
44. Moreth K., Iozzo R.V., Schaefer L. Small leucine-rich proteoglycans orchestrate receptor crosstalk during inflammation. Cell Cycle 2012, 11:2084-2091.
45. Munoz J.R., Stoutenger B.R., Robinson A.P., Spees J.L., Prockop D.J. Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(50):18171-18176. (Dec 13) (Electronic publication ahead of print, 2005 Dec 5).
46. Nandoe R.D., Hurtado A., Levi A.D., Grotenhuis A., Oudega M. Bone marrow stromal cells for repair of the spinal cord: towards clinical application. Cell Transplant. 2006, 15:563-577.
47. Neill T., Painter H., Buraschi S., Owens R.T., Lisanti M.P., Schaefer L., Iozzo R.V. Decorin antagonizes the angiogenic network: concurrent inhibition of Met, hypoxia inducible factor 1α, vascular endothelial growth factor A, and induction of thrombospondin-1 and TIMP3. J. Biol. Chem. 2012, 287:5492-5506.
48. Neuhuber B., Timothy Himes B., Shumsky J.S., Gallo G., Fischer I. Axon growth and recovery of function supported by human bone marrow stromal cells in the injured spinal cord exhibit donor variations. Brain Res. 2005, 1035:73-85.
49. Nishimura T., Futami E., Taneichi A., Mori T., Hattori A. Decorin expression during development of bovine skeletal muscle and its role in morphogenesis of the intramuscular connective tissue. Cells Tissues Organs 2002, 171:199-214.
50. Nishimura T., Nozu K., Kishioka Y., Wakamatsu J., Hattori A. Decorin expression in quiescent myogenic cells. Biochem. Biophys. Res. Commun. 2008, 370:383-387.
51. Oudega M., Varon S., Hagg T. Regeneration of adult rat sensory axons into intraspinal nerve grafts: promoting effects of conditioning lesion and graft predegeneration. Exp. Neurol. 1994, (2):194-206.
52. Phinney D.G., Prockop D.J. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair-current views. Stem Cells 2007, 25:2896-2902.
53. Plant G.W., Currier P.F., Cuervo E.P., Bates M.L., Pressman Y., Bunge M.B., Wood P.M. Purified adult ensheathing glia fail to myelinate axons under culture conditions that enable Schwann cells to form myelin. J. Neurosci. 2002, 22:6083-6091.
54. Plant G.W., Christensen C.L., Oudega M., Bunge M.B. Delayed transplantation of olfactory ensheathing glia promotes sparing/regeneration of supraspinal axons in the contused adult rat spinal cord. J. Neurotrauma 2003, 20:1-16.
55. Quertainmont R., Cantinieaux D., Botman O., Sid S., Schoenen J., Franzen R. Mesenchymal stem cell graft improves recovery after spinal cord injury in adult rats through neurotrophic and pro-angiogenic actions. PLoS One 2012, 7(6):e39500.
56. Ramamurthy P., Hocking A.M., McQuillan D.J. Recombinant decorin glycoforms. Purification and structure. J. Biol. Chem. 1996, 271:19578-19584.
57. Sandvig A., Berry M., Barrett L.B., Butt A., Logan A. Myelin-, reactive glia-, and scar-derived CNS axon growth inhibitors: expression, receptor signaling, and correlation with axon regeneration. Glia 2004, 46:225-251.
58. Santiago-Garcia J., Kodama T., Pitas R.E. The class A scavenger receptor binds to proteoglycans and mediates adhesion of macrophages to the extracellular matrix. J. Biol. Chem. 2003, 278:6942-6946.
59. Sasaki M., Radtke C., Tan A.M., Zhao P., Hamada H., Houkin K., Honmou O., Kocsis J.D. BDNF-hypersecreting human mesenchymal stem cells promote functional recovery, axonal sprouting, and protection of corticospinal neurons after spinal cord injury. J. Neurosci. 2009, 29:14932-14941.
60. Seo N.S., Hocking A.M., Hook M., McQuillan D.J. Decorin core protein secretion is regulated by N-linked oligosaccharide and glycosaminoglycan additions. J. Biol. Chem. 2005, 280:42774-42784.
61. Simmons P.J., Torok-Storb B. Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood 1991, 78:55-62.
62. Singer N.G., Caplan A.I. Mesenchymal stem cells: mechanisms of inflammation. Annu. Rev. Pathol. 2011, 6:457-478.
63. Spaggiari G.M., Capobianco A., Becchetti S., Mingari M.C., Moretta L. Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood 2006, 107:1484-1490.
64. Steeves J.D., Lammertse D., Curt A., Fawcett J.W., Tuszynski M.H., Ditunno J.F., Ellaway P.H., Fehlings M.G., Guest J.D., Kleitman N., Bartlett P.F., Blight A.R., Dietz V., Dobkin B.H., Grossman R., Short D., Nakamura M., Coleman W.P., Gaviria M., Privat A. Guidelines for the conduct of clinical trials for spinal cord injury (SCI) as developed by the ICCP panel: clinical trial outcome measures. Spinal Cord 2007, 45:206-221.
65. Stein M., Keshav S., Harris N., Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med. 1992, 176:287-292.
66. Sykova E., Homola A., Mazanec R., Lachmann H., Konradova S.L., Kobylka P., Padr R., Neuwirth J., Komrska V., Vavra V., Stulik J., Bojar M. Autologous bone marrow transplantation in patients with subacute and chronic spinal cord injury. Cell Transplant. 2006, 15:675-687.
67. Tufvesson E., Westergren-Thorsson G. Tumour necrosis factor-alpha interacts with biglycan and decorin. FEBS Lett. 2002, 530:124-128.
68. Vaquero J., Zurita M., Oya S., Santos M. Cell therapy using bone marrow stromal cells in chronic paraplegic rats: systemic or local administration?. Neurosci. Lett. 2006, 398:129-134.
69. Xaus J., Comalada M., Cardo M., Valledor A.F., Celada A. Decorin inhibits macrophage colony-stimulating factor proliferation of macrophages and enhances cell survival through induction of p27(Kip1) and p21(Waf1). Blood 2001, 98:2124-2133.
70. Yamada H., Watanabe K., Shimonaka M., Yamaguchi Y. Molecular cloning of brevican, a novel brain proteoglycan of the aggrecan/versican family. J. Biol. Chem. 1994, 269:10119-10126.
71. Yamaguchi Y., Mann D.M., Ruoslahti E. Negative regulation of transforming growth factor-beta by the proteoglycan decorin. Nature 1990, 346:281-284.
72. Zurita M., Vaquero J. Functional recovery in chronic paraplegia after bone marrow stromal cells transplantation. Neuroreport 2004, 15:1105-1108.
73. Zurita M., Vaquero J. Bone marrow stromal cells can achieve cure of chronic paraplegic rats: functional and morphological outcome one year after transplantation. Neurosci. Lett. 2006, 402:51-56.
74. Zurita M., Vaquero J., Bonilla C., Santos M., De Haro J., Oya S., Aguayo C. Functional recovery of chronic paraplegic pigs after autologous transplantation of bone marrow stromal cells. Transplantation 2008, 86:845-853.