Transplantation of mesenchymal stem cells promotes tissue regeneration in a glaucoma model through laser-induced paracrine factor secretion and progenitor cell recruitment

Stem Cells

Volumn 31, Issue 6, 2013, Pages 1136-1148

  Manuguerra Gagné, Renaud ^a,b,c   Boulos, Patrick R ^b,c   Ammar, Ahmed ^a,b   Leblond, François A ^a   Krosl, Gorazd ^a   Pichette, Vincent ^a,c   Lesk, Mark R ^b,c   Roy, Denis Claude ^a,c  

^a UNIVERSITY OF MONTREAL   (Canada)

^b MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Bone marrow mononuclear cells; Glaucoma; Intraocular pressure; Mesenchymal stem cells; Tissue regeneration

Indexed keywords

NESTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR EYE CHAMBER; ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSDIFFERENTIATION; CILIARY BODY; CONTROLLED STUDY; HEMATOPOIETIC CELL; INTRAOCULAR PRESSURE; LASER; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; OPEN ANGLE GLAUCOMA; PROTEIN EXPRESSION; TISSUE REGENERATION; TRABECULAR MESHWORK;

ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL GROWTH PROCESSES; CELL MOVEMENT; CELL SURVIVAL; CELLS, CULTURED; CILIARY BODY; DISEASE MODELS, ANIMAL; FEMALE; GLAUCOMA; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; PARACRINE COMMUNICATION; RATS; RATS, INBRED BN; REGENERATION; TRABECULAR MESHWORK;

EID: 84878001547     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1364     Document Type: Article

References (68)

1. Wu Y, Chen L, Scott PG et al. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells 2007;25:2648-2659. (Pubitemid 47582758)
2. Li H, Fu X, Ouyang Y et al. Adult bone-marrow-derived mesenchymal stem cells contribute to wound healing of skin appendages. Cell Tissue Res 2006;326:725-736. (Pubitemid 44786372)
3. Mellough CB, Sernagor E, Moreno-Gimeno I et al. Efficient stage-specific differentiation of human pluripotent stem cells toward retinal photoreceptor cells. Stem Cells 2012;30:673-686.
4. Fujimoto Y, Abematsu M, Falk A et al. Treatment of a mouse model of spinal cord injury by transplantation of human induced pluripotent stem cell-derived long-term self-renewing neuroepithelial-like stem cells. Stem Cells 2012;30:1163-1173.
5. Gnecchi M, Zhang Z, Ni A et al. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 2008;103:1204-1219.
6. Munoz JR, Stoutenger BR, Robinson AP et al. Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc Natl Acad Sci USA 2005;102:18171-18176. (Pubitemid 41798520)
7. Nguyen BK, Maltais S, Perrault LP et al. Improved function and myocardial repair of infarcted heart by intracoronary injection of mesenchymal stem cell-derived growth factors. J Cardiovasc Transl Res 2010;3:547-558.
8. Phinney DG, Prockop DJ.Concise review: Mesenchymal stem/multipotent stromal cells: The state of transdifferentiation and modes of tissue repair-current views. Stem Cells 2007;25:2896-2902. (Pubitemid 350127874)
9. Uccelli A, Moretta L, Pistoia V.Mesenchymal stem cells in health and disease. Nat Rev. Immunol 2008;8:726-736.
10. van Haaften T, Byrne R, Bonnet S et al. Airway delivery of mesenchymal stem cells prevents arrested alveolar growth in neonatal lung injury in rats. Am J Respir Critical Care Med 2009;180:1131-1142.
11. Le Blanc K, Rasmusson I, Sundberg B et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004;363:1439-1441. (Pubitemid 38586721)
12. Pittenger MF, Martin BJ.Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res 2004;95:9-20. (Pubitemid 38931831)
13. Takahashi M, Li TS, Suzuki R et al. Cytokines produced by bone marrow cells can contribute to functional improvement of the infarcted heart by protecting cardiomyocytes from ischemic injury. Am J Physiol Heart Circ Physiol 2006;291:H886-H893. (Pubitemid 44175098)
14. Togel F, Hu Z, Weiss K et al. Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol 2005;289:F31-F42. (Pubitemid 40863570)
15. Ninichuk V, Gross O, Segerer S et al. Multipotent mesenchymal stem cells reduce interstitial fibrosis but do not delay progression of chronic kidney disease in collagen4A3-deficient mice. Kidney Int 2006;70:121-129. (Pubitemid 44000128)
16. Wang W, Jiang Q, Zhang H et al. Intravenous administration of bone marrow mesenchymal stromal cells is safe for the lung in a chronic myocardial infarction model. Regen Med 2011;6:179-190.
17. Levin LA, Ritch R, Richards JE et al. Stem cell therapy for ocular disorders. Arch Ophthalmol 2004;122:621-627. (Pubitemid 38456299)
18. Quigley HA.Open-angle glaucoma. New Engl J Med 1993;328:1097-1106. (Pubitemid 23097800)
19. Acott TS, Kelley MJ.Extracellular matrix in the trabecular meshwork. Exp Eye Res 2008;86:543-561.
20. Alvarado J, Murphy C, Polansky J et al. Age-related changes in trabecular meshwork cellularity. Invest Ophthalmol Vis Sci 1981;21:714-727. (Pubitemid 12229217)
21. Baleriola J, Garcia-Feijoo J, Martinez-de-la-Casa JM et al. Apoptosis in the trabecular meshwork of glaucomatous patients. Mol Vis 2008;14:1513-1516.
22. Caballero M, Liton PB, Epstein DL et al. Proteasome inhibition by chronic oxidative stress in human trabecular meshwork cells. Biochem Biophys Res Commun 2003;308:346-352. (Pubitemid 36937186)
23. Grierson I, Howes RC.Age-related depletion of the cell population in the human trabecular meshwork. Eye 1987;1(pt 2):204-210. (Pubitemid 17133335)
24. Tamm ER.The trabecular meshwork outflow pathways: Structural and functional aspects. Exp Eye Res 2009;88:648-655.
25. Tamm ER, Fuchshofer R.What increases outflow resistance in primary open-angle glaucoma? Survey Ophthalmol 2007;52(suppl 2):S101-S104. (Pubitemid 350060958)
26. Kwon YH, Fingert JH, Kuehn MH et al. Primary open-angle glaucoma. New Engl J Med 2009;360:1113-1124.
27. Chauhan BC, Mikelberg FS, Artes PH et al. Canadian Glaucoma Study: 3. Impact of risk factors and intraocular pressure reduction on the rates of visual field change. Arch Ophthalmol 2010;128:1249-1255.
28. Leske MC, Wu SY, Hennis A et al. Risk factors for incident open-angle glaucoma: The Barbados Eye Studies. Ophthalmology 2008;115:85-93. (Pubitemid 350309410)
29. Leske MC, Wu SY, Honkanen R et al. Nine-year incidence of open-angle glaucoma in the Barbados Eye Studies. Ophthalmology 2007;114:1058-1064. (Pubitemid 46829370)
30. McKinnon SJ, Goldberg LD, Peeples P et al. Current management of glaucoma and the need for complete therapy. Am J Manag Care 2008;14:S20-S27. (Pubitemid 351341925)
31. Robert MC, Hamel P, Blondeau P et al. Persistent leak after glaucoma aqueous shunt implantation. J Glaucoma [Epub ahead of print].
32. Tamm ER, Russell P, Piatigorsky J.Development of characterization of a immortal and differentiated murine trabecular meshwork cell line. Invest Ophthalmol Vis Sci 1999;40:1392-1403. (Pubitemid 29252330)
33. Levkovitch-Verbin H, Quigley HA, Martin KR et al. Translimbal laser photocoagulation to the trabecular meshwork as a model of glaucoma in rats. Invest Ophthalmol Vis Sci 2002;43:402-410. (Pubitemid 34113222)
34. Gabelt BT, Seeman JL, Podos SM et al. Aqueous humor dynamics in monkeys after topical 8-iso PGE(2). Invest Ophthalmol Vis Sci 2004;45:892-899. (Pubitemid 38868388)
35. Shruster A, Ben-Zur T, Melamed E et al. Wnt signaling enhances neurogenesis and improves neurological function after focal ischemic injury. Plos One 2012;7:e40843.
36. Mansour S, Roy DC, Bouchard V et al. COMPARE-AMI trial: Comparison of intracoronary injection of CD133+ bone marrow stem cells to placebo in patients after acute myocardial infarction and left ventricular dysfunction: Study rationale and design. J Cardiovasc Transl Res 2010;3:153-159.
37. Herrmann JL, Wang Y, Abarbanell AM et al. Preconditioning mesenchymal stem cells with transforming growth factor-alpha improves mesenchymal stem cell-mediated cardioprotection. Shock 2010;33:24-30.
38. Rosova I, Dao M, Capoccia B et al. Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells 2008;26:2173-2182.
39. Trivedi P, Tray N, Nguyen T et al. Mesenchymal stem cell therapy for treatment of cardiovascular disease: Helping people sooner or later. Stem Cells Dev 2010;19:1109-1120.
40. Abdouh M, Bernier G.In vivo reactivation of a quiescent cell population located in the ocular ciliary body of adult mammals. Exp Eye Res 2006;83:153-164. (Pubitemid 43783245)
41. Bhatia B, Singhal S, Lawrence JM et al. Distribution of Muller stem cells within the neural retina: Evidence for the existence of a ciliary margin-like zone in the adult human eye. Exp Eye Res 2009;89:373-382.
42. London A, Itskovich E, Benhar I et al. Neuroprotection and progenitor cell renewal in the injured adult murine retina requires healing monocyte-derived macrophages. J Exp Med 2011;208:23-39.
43. Martinez-Navarrete GC, Angulo A, Martin-Nieto J et al. Gradual morphogenesis of retinal neurons in the peripheral retinal margin of adult monkeys and humans. J Comp Neurol 2008;511:557-580.
44. MacNeil A, Pearson RA, MacLaren RE et al. Comparative analysis of progenitor cells isolated from the iris, pars plana, and ciliary body of the adult porcine eye. Stem Cells 2007;25:2430-2438. (Pubitemid 47582735)
45. Ohta K, Ito A, Tanaka H.Neuronal stem/progenitor cells in the vertebrate eye. Development, Growth Differ 2008;50:253-259. (Pubitemid 351661156)
46. Xu H, Sta Iglesia DD, Kielczewski JL et al. Characteristics of progenitor cells derived from adult ciliary body in mouse, rat, and human eyes. Invest Ophthalmol Vis Sci 2007;48:1674-1682. (Pubitemid 351261353)
47. de Smet MD, Gunning F, Feenstra R.The surgical management of chronic hypotony due to uveitis. Eye 2005;19:60-64. (Pubitemid 40192641)
48. Willermain F, Rosenbaum JT, Bodaghi B et al. Interplay between innate and adaptive immunity in the development of non-infectious uveitis. Progr Retinal Eye Res 2012;31:182-194.
49. Kerr EC, Copland DA, Dick AD et al. The dynamics of leukocyte infiltration in experimental autoimmune uveoretinitis. Progr Retinal Eye Res 2008;27:527-535.
50. Johnson TV, Bull ND, Hunt DP et al. Neuroprotective effects of intravitreal mesenchymal stem cell transplantation in experimental glaucoma. Invest Ophthalmol Vis Sci 2010;51:2051-2059.
51. Duffield JS, Park KM, Hsiao LL et al. Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. J Clin Invest 2005;115:1743-1755. (Pubitemid 40979713)
52. Gnecchi M, He H, Noiseux N et al. Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J 2006;20:661-669. (Pubitemid 44933310)
53. Noiseux N, Gnecchi M, Lopez-Ilasaca M et al. Mesenchymal stem cells overexpressing Akt dramatically repair infarcted myocardium and improve cardiac function despite infrequent cellular fusion or differentiation. Mol Ther 2006;14:840-850. (Pubitemid 44752717)
54. Copland IB, Galipeau J.Death and inflammation following somatic cell transplantation. Semin Immunopathol 2011;33:535-550.
55. Aggarwal S, Pittenger MF.Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105:1815-1822. (Pubitemid 40223708)
56. Block GJ, Ohkouchi S, Fung F et al. Multipotent stromal cells are activated to reduce apoptosis in part by upregulation and secretion of stanniocalcin-1. Stem Cells 2009;27:670-681.
57. Djouad F, Bouffi C, Ghannam S et al. Mesenchymal stem cells: Innovative therapeutic tools for rheumatic diseases. Nat Rev Rheumatol 2009;5:392-399.
58. Groh ME, Maitra B, Szekely E et al. Human mesenchymal stem cells require monocyte-mediated activation to suppress alloreactive T cells. Exp Hematol 2005;33:928-934. (Pubitemid 40982660)
59. Hatzistergos KE, Quevedo H, Oskouei BN et al. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res 2010;107:913-922.
60. Nagaya N, Fujii T, Iwase T et al. Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis. Am J Physiol Heart Circ Physiol 2004;287:H2670-H2676. (Pubitemid 39557139)
61. Uccelli A, Prockop DJ.Why should mesenchymal stem cells (MSCs) cure autoimmune diseases? Curr Opin Immunol 2010;22:768-774.
62. Li L, Zhang S, Zhang Y et al. Paracrine action mediate the antifibrotic effect of transplanted mesenchymal stem cells in a rat model of global heart failure. Mol Biol Rep 2009;36:725-731.
63. Beguin PC, El-Helou V, Gillis MA et al. Nestin (+) stem cells independently contribute to neural remodelling of the ischemic heart. J Cell Physiol 2011;226:1157-1165.
64. Bhatia B, Jayaram H, Singhal S et al. Differences between the neurogenic and proliferative abilities of Muller glia with stem cell characteristics and the ciliary epithelium from the adult human eye. Exp Eye Res 2011;93:852-861.
65. Wiese C, Rolletschek A, Kania G et al. Nestin expression - A property of multi-lineage progenitor cells? Cell Mol Life Sci 2004;61:2510-2522. (Pubitemid 39586514)
66. Bocker W, Docheva D, Prall WC et al. IKK-2 is required for TNF-alpha-induced invasion and proliferation of human mesenchymal stem cells. J Mol Med 2008;86:1183-1192.
67. Liu ZJ, Zhuge Y, Velazquez OC.Trafficking and differentiation of mesenchymal stem cells. J Cell Biochem 2009;106:984-991.
68. Zhang M, Mal N, Kiedrowski M et al. SDF-1 expression by mesenchymal stem cells results in trophic support of cardiac myocytes after myocardial infarction. FASEB J 2007;21:3197-3207. (Pubitemid 47565538)