Low-dose curcumin stimulates proliferation, migration and phagocytic activity of olfactory ensheathing cells

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Velasquez, Johana Tello ^a   Watts, Michelle E ^a   Todorovic, Michael ^a   Nazareth, Lynnmaria ^a,b   Pastrana, Erika ^c   Diaz Nido, Javier ^d   Lim, Filip ^e   Ekberg, Jenny A K ^a,b   Quinn, Ronald J ^a   St John, James A ^a  

^a GRIFFITH UNIVERSITY   (Australia)

^b QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^c Nature Communications   (United States)

^d CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^e UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CURCUMIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL PHAGOCYTOSIS; CELL PROLIFERATION; CELL TRANSPLANTATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; MOUSE; NERVE REGENERATION; NONHUMAN; OLFACTORY ENSHEATHING CELL; ANIMAL; CELL CULTURE; CELL MOTION; CELL SEPARATION; CELL SHAPE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE ONTOLOGY; GLIA; MALE; OLFACTORY BULB; OLFACTORY EPITHELIUM; PHAGOCYTOSIS; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CELL SEPARATION; CELL SHAPE; CELLS, CULTURED; CURCUMIN; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE ONTOLOGY; MALE; MICE, TRANSGENIC; NEUROGLIA; OLFACTORY BULB; OLFACTORY MUCOSA; PHAGOCYTOSIS; SIGNAL TRANSDUCTION;

EID: 84909991723     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0111787     Document Type: Article

References (75)

1. Chuah MI, Hale DM, West AK (2011) Interaction of olfactory ensheathing cells with other cell types in vitro and after transplantation: glial scars and inflammation. Exp Neurol 229: 46-53.
2. Roet KC, Franssen EH, de Bree FM, Essing AH, Zijlstra SJ, et al. (2013) A Multilevel Screening Strategy Defines a Molecular Fingerprint of Proregenerative Olfactory Ensheathing Cells and Identifies SCARB2, a Protein That Improves Regenerative Sprouting of Injured Sensory Spinal Axons. J Neurosci 33: 11116-11135.
3. Garcia-Escudero V, Garcia-Gomez A, Langa E, Martin-Bermejo MJ, Ramirez-Camacho R, et al. (2012) Patient-derived olfactory mucosa cells but not lung or skin fibroblasts mediate axonal regeneration of retinal ganglion neurons. Neuroscience Letters 509: 27-32.
4. Sandvig I, Hoang L, Sardella TCP, Barnett SC, Brekken C, et al. (2012) Labelling of olfactory ensheathing cells with micron-sized particles of iron oxide and detection by MRI. Contrast Media & Molecular Imaging 7: 403-410.
5. Simon D, Martin-Bermejo MJ, Gallego-Hernandez MT, Pastrana E, Garcia-Escudero V, et al. (2011) Expression of plasminogen activator inhibitor-1 by olfactory ensheathing glia promotes axonal regeneration. Glia 59: 1458-1471.
6. Su ZD, Chen JJ, Qiu Y, Yuan YM, Zhu F, et al. (2013) Olfactory ensheathing cells: The primary innate immunocytes in the olfactory pathway to engulf apoptotic olfactory nerve debris. Glia 61: 490-503.
7. Wewetzer K, Kern N, Ebel C, Radtke C, Brandes G (2005) Phagocytosis of O4(+) axonal fragments in vitro by p75(-) neonatal rat olfactory ensheathing cells. Glia 49: 577-587.
8. Lankford KL, Sasaki M, Radtke C, Kocsis JD (2008) Olfactory ensheathing cells exhibit unique migratory, phagocytic, and myelinating properties in the X-irradiated spinal cord not shared by Schwann cells. Glia 56: 1664-1678.
9. Panni P, Ferguson IA, Beacham I, Mackay-Sim A, Ekberg JA, et al. (2013) Phagocytosis of bacteria by olfactory ensheathing cells and Schwann cells. Neuroscience Letters 539: 65-70.
10. Leung JY, Chapman JA, Harris JA, Hale D, Chung RS, et al. (2008) Olfactory ensheathing cells are attracted to, and can endocytose, bacteria. Cell Mol Life Sci 65: 2732-2739.
11. Su Z, Yuan Y, Chen J, Cao L, Zhu Y, et al. (2009) Reactive astrocytes in glial scar attract olfactory ensheathing cells migration by secreted TNF-alpha in spinal cord lesion of rat. PLoS One 4: e8141.
12. Lakatos A, Franklin RJM, Barnett SC (2000) Olfactory ensheathing cells and Schwann cells differ in their in vitro interactions with astrocytes. Glia 32: 214-225.
13. Li Y, Field PM, Raisman G (1997) Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 277: 2000-2002.
14. Ramon-Cueto A (2000) Olfactory ensheathing glia transplantation into the injured spinal cord. Neural Plasticity and Regeneration 128: 265-272.
15. Li Y, Sauve Y, Li D, Lund RD, Raisman G (2003) Transplanted olfactory ensheathing cells promote regeneration of cut adult rat optic nerve axons. J Neurosci 23: 7783-7788.
16. Stamegna JC, Felix MS, Roux-Peyronnet J, Rossi V, Feron F, et al. (2011) Nasal OEC transplantation promotes respiratory recovery in a subchronic rat model of cervical spinal cord contusion. Experimental Neurology 229: 120-131.
17. Su Z, He C (2010) Olfactory ensheathing cells: biology in neural development and regeneration. Prog Neurobiol 92: 517-532.
18. Granger N, Blamires H, Franklin RJ, Jeffery ND (2012) Autologous olfactory mucosal cell transplants in clinical spinal cord injury: a randomized double-blinded trial in a canine translational model. Brain 135: 3227-3237.
19. Yang H, He BR, Hao DJ (2014) Biological Roles of Olfactory Ensheathing Cells in Facilitating Neural Regeneration: A Systematic Review. Mol Neurobiol.
20. Lu P, Yang H, Culbertson M, Graham L, Roskams AJ, et al. (2006) Olfactory ensheathing cells do not exhibit unique migratory or axonal growth-promoting properties after spinal cord injury. Journal of Neuroscience 26: 11120-11130.
21. Lima C, Pratas-Vital J, Escada P, Hasse-Ferreira A, Capucho C, et al. (2006) Olfactory mucosa autografts in human spinal cord injury: A pilot clinical study. Journal of Spinal Cord Medicine 29: 191-203.
22. Feron F, Perry C, Cochrane J, Licina P, Nowitzke A, et al. (2005) Autologous olfactory ensheathing cell transplantation in human spinal cord injury. Brain 128: 2951-2960.
23. Li L, Adnan H, Xu B, Wang J, Wang C, et al. (2014) Effects of transplantation of olfactory ensheathing cells in chronic spinal cord injury: a systematic review and meta-analysis. European Spine Journal.
24. Hatcher H, Planalp R, Cho J, Tortia FM, Torti SV (2008) Curcumin: From ancient medicine to current clinical trials. Cellular and Molecular Life Sciences 65: 1631-1652.
25. Wilken R, Veena MS, Wang MB, Srivatsan ES (2011) Curcumin: A review of anti-cancer properties and therapeutic activity in head and neck squamous cell carcinoma. Molecular Cancer 10.
26. Liao KK, Wu MJ, Chen PY, Huang SW, Chiu SJ, et al. (2012) Curcuminoids Promote Neurite Outgrowth in PC12 Cells through MAPK/ERK- and PKC-Dependent Pathways. Journal of Agricultural and Food Chemistry 60: 433-443.
27. Kim SJ, Son TG, Park HR, Park M, Kim MS, et al. (2008) Curcumin stimulates proliferation of embryonic neural progenitor cells and neurogenesis in the adult hippocampus. Journal of Biological Chemistry 283: 14497-14505.
28. Patzko A, Bai YH, Saporta MA, Katona I, Wu XY, et al. (2012) Curcumin derivatives promote Schwann cell differentiation and improve neuropathy in R98C CMT1B mice. Brain 135: 3551-3566.
29. Ormond DR, Peng H, Zeman R, Das K, Murali R, et al. (2012) Recovery from spinal cord injury using naturally occurring antiinflammatory compound curcumin Laboratory investigation. Journal of Neurosurgery-Spine 16: 497-503.
30. Kavakli HS, Koca C, Alici O (2011) Antioxidant effects of curcumin in spinal cord injury in rats. Ulusal Travma Ve Acil Cerrahi Dergisi-Turkish Journal of Trauma & Emergency Surgery 17: 14-18.
31. Lin MS, Lee YH, Chiu WT, Hung KS (2011) Curcumin Provides Neuroprotection After Spinal Cord Injury. Journal of Surgical Research 166: 280-289.
32. Ekberg JA, Amaya D, Chehrehasa F, Lineburg K, Claxton C, et al. (2011) OMP-ZsGreen fluorescent protein transgenic mice for visualisation of olfactory sensory neurons in vivo and in vitro. J Neurosci Methods 196: 88-98.
33. Windus LC, Claxton C, Allen CL, Key B, St John JA (2007) Motile membrane protrusions regulate cell-cell adhesion and migration of olfactory ensheathing glia. Glia 55: 1708-1719.
34. Tripathi RB, Mctigue DM (2008) Chronically increased ciliary neurotrophic factor and fibroblast growth factor-2 expression after spinal contusion in rats. Journal of Comparative Neurology 510: 129-144.
35. Edelmann K, Glashauser L, Sprungala S, Hesl B, Fritschle M, et al. (2013) Increased radial glia quiescence, decreased reactivation upon injury and unaltered neuroblast behavior underlie decreased neurogenesis in the aging zebrafish telencephalon. J Comp Neurol 521: 3099-3115.
36. Ramon-Cueto A, Nieto-Sampedro M (1992) Glial cells from adult rat olfactory bulb: immunocytochemical properties of pure cultures of ensheathing cells. Neuroscience 47: 213-220.
37. Franceschini IA, Barnett SC (1996) Low-affinity NGF-receptor and E-N-CAM expression define two types of olfactory nerve ensheathing cells that share a common lineage. Dev Biol 173: 327-343.
38. Kim DW, Uetsuki T, Kaziro Y, Yamaguchi N, Sugano S (1990) Use of the Human Elongation Factor-1-Alpha Promoter as a Versatile and Efficient Expression System. Gene 91: 217-223.
39. Moreno-Flores MT, Lim F, Martin-Bermejo MJ, Diaz-Nido J, Avila J, et al. (2003) Immortalized olfactory ensheathing glia promote axonal regeneration of rat retinal ganglion neurons. Journal of Neurochemistry 85: 861-871.
40. Windus LC, Chehrehasa F, Lineburg KE, Claxton C, Mackay-Sim A, et al. (2011) Stimulation of olfactory ensheathing cell motility enhances olfactory axon growth. Cell Mol Life Sci 68: 3233-3247.
41. Windus LC, Lineburg KE, Scott SE, Claxton C, Mackay-Sim A, et al. (2010) Lamellipodia mediate the heterogeneity of central olfactory ensheathing cell interactions. Cell Mol Life Sci 67: 1735-1750.
42. Cholfin JA, Rubenstein JLR (2008) Frontal cortex subdivision patterning is coordinately regulated by Fgf8, Fgf17, and Emx2. Journal of Comparative Neurology 509: 144-155.
43. Yamada J, Jinno S (2013) Novel objective classification of reactive microglia following hypoglossal axotomy using hierarchical cluster analysis. Journal of Comparative Neurology 521: 1184-1201.
44. Huang TY, Tsai TH, Hsu CW, Hsu YC (2010) Curcuminoids suppress the growth and induce apoptosis through caspase-3-dependent pathways in glioblastoma multiforme (GBM) 8401 cells. J Agric Food Chem 58: 10639-10645.
45. Yan H, Lu D, Rivkees SA (2003) Lysophosphatidic acid regulates the proliferation and migration of olfactory ensheathing cells in vitro. Glia 44: 26-36.
46. Weir NM, Selvendiran K, Kutala VK, Tong LY, Vishwanath S, et al. (2007) Curcumin induces G2/M arrest and apoptosis in cisplatin-resistant human ovarian cancer cells by modulating Akt and p38 MAPK. Cancer Biology & Therapy 6: 178-184.
47. Goel A, Kunnumakkara AB, Aggarwal BB (2008) Curcumin as "Curecumin": From kitchen to clinic. Biochemical Pharmacology 75: 787-809.
48. Watson JL, Greenshields A, Hill R, Hilchie A, Lee PW, et al. (2010) Curcumin-Induced Apoptosis in Ovarian Carcinoma Cells Is p53-Independent and Involves p38 Mitogen-Activated Protein Kinase Activation and Downregulation of Bcl-2 and Survivin Expression and Akt Signaling. Molecular Carcinogenesis 49: 13-24.
49. Goel A, Jhurani S, Aggarwal BB (2008) Multi-targeted therapy by curcumin: how spicy is it? Molecular Nutrition & Food Research 52: 1010-1030.
50. Calvano SE, Xiao WZ, Richards DR, Felciano RM, Baker HV, et al. (2005) A network-based analysis of systemic inflammation in humans. Nature 437: 1032-1037.
51. Bisht K, Choi WH, Park SY, Chung MK, Koh WS (2009) Curcumin enhances non-inflammatory phagocytic activity of RAW264.7 cells. Biochemical and Biophysical Research Communications 379: 632-636.
52. Mimche PN, Thompson E, Taramelli D, Vivas L (2012) Curcumin enhances non-opsonic phagocytosis of Plasmodium falciparum through up-regulation of CD36 surface expression on monocytes/macrophages. Journal of Antimicrobial Chemotherapy 67: 1895-1904.
53. Rogers NM, Kireta S, Coates PTH (2010) Curcumin induces maturationarrested dendritic cells that expand regulatory T cells in vitro and in vivo. Clinical and Experimental Immunology 162: 460-473.
54. Zhou HY, Beevers CS, Huang SL (2011) The Targets of Curcumin. Current Drug Targets 12: 332-347.
55. He BR, Xie ST, Wu MM, Hao DJ, Yang H (2014) Phagocytic removal of neuronal debris by olfactory ensheathing cells enhances neuronal survival and neurite outgrowth via p38MAPK activity. Mol Neurobiol 49: 1501-1512.
56. Kang ES, Woo IS, Kim HJ, Eun SY, Paek KS, et al. (2007) Up-regulation of aldose reductase expression mediated by phosphatidylinositol 3-kinase/Akt and Nrf2 is involved in the protective effect of curcumin against oxidative damage. Free Radical Biology and Medicine 43: 535-545.
57. David S, Aguayo AJ (1981) Axonal Elongation into Peripheral Nervous-System Bridges after Central Nervous-System Injury in Adult-Rats. Science 214: 931-933.
58. David S, Kroner A (2011) Repertoire of microglial and macrophage responses after spinal cord injury. Nature Reviews Neuroscience 12: 388-399.
59. Ladeby R, Wirenfeldt M, Dalmau I, Gregersen R, Garcia-Ovejero D, et al. (2005) Proliferating resident microglia express the stem cell antigen CD34 in response to acute neural injury. Glia 50: 121-131.
60. Huizinga R, van der Star BJ, Kipp M, Jong R, Gerritsen W, et al. (2012) Phagocytosis of neuronal debris by microglia is associated with neuronal damage in multiple sclerosis. Glia 60: 422-431.
61. Vincent AJ, West AK, Chuah MI (2005) Morphological and functional plasticity of olfactory ensheathing cells. Journal of Neurocytology 34: 65-80.
62. Woodhall E, West AK, Vickers JC, Chuah MI (2003) Olfactory ensheathing cell phenotype following implantation in the lesioned spinal cord. Cellular and Molecular Life Sciences 60: 2241-2253.
63. Doucette R (1995) Olfactory Ensheathing Cells - Potential for Glial-Cell Transplantation into Areas of Cns Injury. Histology and Histopathology 10: 503-507.
64. Huang ZH, Wang Y, Cao L, Su ZD, Zhu YL, et al. (2008) Migratory properties of cultured olfactory ensheathing cells by single-cell migration assay. Cell Research 18: 479-490.
65. Chehrehasa F, Windus LC, Ekberg JA, Scott SE, Amaya D, et al. (2010) Olfactory glia enhance neonatal axon regeneration. Mol Cell Neurosci 45: 277-288.
66. Liu Y, Gong ZL, Liu L, Sun HJ (2010) Combined effect of olfactory ensheathing cell (OEC) transplantation and glial cell line-derived neurotrophic factor (GDNF) intravitreal injection on optic nerve injury in rats. Molecular Vision 16: 2903-2910.
67. Cao L, Liu L, Chen ZY, Wang LM, Ye JL, et al. (2004) Olfactory ensheathing cells genetically modified to secrete GDNF to promote spinal cord repair. Brain 127: 535-549.
68. St John JA, Key B (2003) Axon mis-targeting in the olfactory bulb during regeneration of olfactory neuroepithelium. Chemical Senses 28: 773-779.
69. Lipson AC, Widenfalk J, Lindqvist E, Ebendal T, Olson L (2003) Neurotrophic properties of olfactory ensheathing glia. Experimental Neurology 180: 167-171.
70. Ireson CR, Jones DJL, Orr S, Coughtrie MWH, Boocock DJ, et al. (2002) Metabolism of the cancer chemopreventive agent curcumin in human and rat intestine. Cancer Epidemiology Biomarkers & Prevention 11: 105-111.
71. Sharma RA, Gescher AJ, Steward WP (2005) Curcumin: The story so far. European Journal of Cancer 41: 1955-1968.
72. Sharma RA, Euden SA, Platton SL, Cooke DN, Shafayat A, et al. (2004) Phase I clinical trial of oral curcumin: Biomarkers of systemic activity and compliance. Clinical Cancer Research 10: 6847-6854.
73. Anand P, Nair HB, Sung BK, Kunnumakkara AB, Yadav VR, et al. (2010) Design of curcumin-loaded PLGA nanoparticles formulation with enhanced cellular uptake, and increased bioactivity in vitro and superior bioavailability in vivo. Biochemical Pharmacology 79: 330-338.
74. Marczylo TH, Verschoyle RD, Cooke DN, Morazzoni P, Steward WP, et al. (2007) Comparison of systemic availability of curcumin with that of curcumin formulated with phosphatidylcholine. Cancer Chemotherapy and Pharmacology 60: 171-177.
75. Adams BK, Ferstl EM, Davis MC, Herold M, Kurtkaya S, et al. (2004) Synthesis and biological evaluation of novel curcumin analogs as anti-cancer and anti-angiogenesis agents. Bioorganic & Medicinal Chemistry 12: 3871-3883.