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01-04-2017 | Original Article

Lipopolysaccharide and Curcumin Co-Stimulation Potentiates Olfactory Ensheathing Cell Phagocytosis Via Enhancing Their Activation

Authors: Ding-Jun Hao, Cuicui Liu, Lingling Zhang, Bo Chen, Qian Zhang, Rui Zhang, Jing An, Jingjing Zhao, Mingmei Wu, Yi Wang, Alfred Simental, Baorong He, Hao Yang

Published in: Neurotherapeutics | Issue 2/2017

Abstract

The gradual deterioration following central nervous system (CNS) injuries or neurodegenerative disorders is usually accompanied by infiltration of degenerated and apoptotic neural tissue debris. A rapid and efficient clearance of these deteriorated cell products is of pivotal importance in creating a permissive environment for regeneration of those damaged neurons. Our recent report revealed that the phagocytic activity of olfactory ensheathing cells (OECs) can make a substantial contribution to neuronal growth in such a hostile environment. However, little is known about how to further increase the ability of OECs in phagocytosing deleterious products. Here, we used an in vitro model of primary cells to investigate the effects of lipopolysaccharide (LPS) and curcumin (CCM) co-stimulation on phagocytic activity of OECs and the possible underlying mechanisms. Our results showed that co-stimulation using LPS and CCM can significantly enhance the activation of OECs, displaying a remarkable up-regulation in chemokine (C-X-C motif) ligand 1, chemokine (C-X-C motif) ligand 2, tumor necrosis factor-α, and Toll-like receptor 4, increased OEC proliferative activity, and improved phagocytic capacity compared with normal and LPS- or CCM-treated OECs. More importantly, this potentiated phagocytosis activity greatly facilitated neuronal growth under hostile culture conditions. Moreover, the up-regulation of transglutaminase-2 and phosphatidylserine receptor in OECs activated by LPS and CCM co-stimulation are likely responsible for mechanisms underlying the observed cellular events, because cystamine (a specific inhibitor of transglutaminase-2) and neutrophil elastase (a cleavage enzyme of phosphatidylserine receptor) can effectively abrogate all the positive effects of OECs, including phagocytic capacity and promotive effects on neuronal growth. This study provides an alternative strategy for the repair of traumatic nerve injury and neurologic diseases with the application of OECs in combination with LPS and CCM.

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Woodhall E, West AK, Chuah MI. Cultured olfactory ensheathing cells express nerve growth factor, brain-derived neurotrophic factor, glia cell line-derived neurotrophic factor and their receptors. Brain Res Mol Brain Res 2001;88:203–213.PubMed

Chung RS, Woodhouse A, Fung S, et al. Olfactory ensheathing cells promote neurite sprouting of injured axons in vitro by direct cellular contact and secretion of soluble factors. Cell Mol Life Sci 2004;61:1238–1245PubMed

Pastrana E, Moreno-Flores MT, Avila J, Wandosell F, Minichiello L, Diaz-Nido J. BDNF production by olfactory ensheathing cells contributes to axonal regeneration of cultured adult CNS neurons. Neurochem Int 2007;50:491-8.PubMed

Roet KC, Verhaagen J. Understanding the neural repair-promoting properties of olfactory ensheathing cells. Exp Neurol 2014;261:594-609PubMed

Lipson AC, Widenfalk J, Lindqvist E, Ebendal T, Olson L. Neurotrophic properties of olfactory ensheathing glia. Exp Neurol 2003;180:167-71.PubMed

Witheford M, Westendorf K, Roskams AJ. Olfactory ensheathing cells promote corticospinal axonal outgrowth by a L1 CAM-dependent mechanism. Glia 2013;61:1873-89.PubMed

Srivastava N, Seth K, Khanna VK, Ansari RW, Agrawal AK. Long-term functional restoration by neural progenitor cell transplantation in rat model of cognitive dysfunction: co-transplantation with olfactory ensheathing cells for neurotrophic factor support. Int J Dev Neurosci 2009;27:103-110.PubMed

He BR, Xie ST, Wu MM, Hao DJ, Yang H. Phagocytic removal of neuronal debris by olfactory ensheathing cells enhances neuronal survival and neurite outgrowth via p38MAPK activity. Mol Neurobiol 2014;49:1501-1512.PubMed

Su Z, Chen J, Qiu Y, et al. Olfactory ensheathing cells: the primary innate immunocytes in the olfactory pathway to engulf apoptotic olfactory nerve debris. Glia 2013;61:490-50.PubMed

10.

Wanner IB, Deik A, Torres M, et al. A new in vitro model of glial scar inhibits axon growth. Glia 2008;56:1691-1709PubMedPubMedCentral

11.

Wanner IB, Anderson MA, Song B, et al. Glial scar borders are formed by newly proliferated, elongated astrocytes that interact to corral inflammatory and fibrotic cells via STAT3-dependent mechanisms after spinal injury. J Neurosci 2013;33:12870-12886PubMedPubMedCentral

12.

Riddell JS, Enriquez-Denton M, Toft A, Fairless R, Barnett SC. Olfactory ensheathing cell grafts have minimal influence on regeneration at the dorsal root entry zone following rhizotomy Glia 2004; 47:150-167.PubMed

13.

Lu P, Yang H, Culbertson M, Graham L, Roskams AJ, Tuszynski MH. Olfactory ensheathing cells do not exhibit unique migratory or axonal growth-promoting properties after spinal cord injury. J Neurosci 2006;26:11120-11130PubMedPubMedCentral

14.

Mukhopadhyay G, Doherty P, Walsh FS, Crocker PR, Filbin MT. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 1994;13:757–767.PubMed

15.

Chen MS, Huber AB, van der Haar ME, et al. Nogo-A is a myelin associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 2000;403:434–439PubMed

16.

Wang KC, Koprivica V, Kim JA, et al. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 2002;417:941–944PubMed

17.

Hata K, Fujitani M, Yasuda Y, et al. RGMa inhibition promotes axonal growth and recovery after spinal cord injury. J Cell Biol 2006;173:47–58PubMedPubMedCentral

18.

Tanaka T, Ueno M, Yamashita T. Engulfment of axon debris by microglia requires p38 MAPK activity. J Biol Chem 2009;284:21626–21636PubMedPubMedCentral

19.

Hulsebosch CE. Recent advances in pathophysiology and treatment of spinal cord injury. Adv Physiol Educ 2002; 26:238–255PubMed

20.

Li S, Liu BP, Budel S, et al. Blockade of Nogo-66, myelin-associated glycoprotein, and oligodendrocyte myelin glycoprotein by soluble Nogo-66 receptor promotes axonal sprouting and recovery after spinal injury. J Neurosci 2004; 24:10511–10520.PubMedPubMedCentral

21.

Fleming JC, Norenberg MD, Ramsay DA, et al. The cellular inflammatory response in human spinal cords after injury. Brain 2006; 129:3249–3269.PubMed

22.

Lauber K, Blumenthal SG, Waibel M, Wesselborg S. Clearance of apoptotic cells: getting rid of the corpses. Mol Cell 2004; 14:277–228.PubMed

23.

Panni P, Ferguson IA, Beacham I, Mackay-Sim A, Ekberg JA, St John JA. Phagocytosis of bacteria by olfactory ensheathing cells and Schwann cells. Neurosci Lett 2013; 539:65-70.PubMed

24.

Nazareth L, Lineburg KE, Chuah MI, et al. Olfactory ensheathing cells are the main phagocytic cells that remove axon debris during early development of the olfactory system. J Comp Neurol 2015; 523:479-494PubMed

25.

Nazareth L, Tello Velasquez J, Lineburg KE, Chehrehasa F, St John JA, Ekberg JA. Differing phagocytic capacities of accessory and main olfactory ensheathing cells and the implication for olfactory glia transplantation therapies. Mol Cell Neurosci 2015; 65:92-101PubMed

26.

Leung JY, Chapman JA, Harris JA, et al. Olfactory ensheathing cells are attracted to, and can endocytose, bacteria. Cell Mol Life Sci 2008; 65:2732–2739PubMed

27.

Kulp A, Kuehn MJ. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 2010; 64:163-184.PubMedPubMedCentral

28.

Mansoor UF, Vitharana D, Reddy PA, et al. Design and synthesis of potent Gram-negative specific LpxC inhibitors. Bioorg Med Chem Lett 2011;21:1155-1161PubMed

29.

Tsatsanis C, Zacharioudaki V, Androulidaki A, et al. Adiponectin induces TNF-alpha and IL-6 in macrophages and promotes tolerance to itself and other pro-inflammatory stimuli. Biochem Biophys Res Commun 2005;335:1254-1263.PubMed

30.

Gertsch J. Anti-inflammatory cannabinoids in diet: Towards a better understanding of CB(2) receptor action? Commun Integr Biol 2008; 1:26-28.PubMedPubMedCentral

31.

Vincent AJ, Taylor JM, Choi-Lundberg DL, West AK, Chuah MI. Genetic expression profile of olfactory ensheathing cells is distinct from that of Schwann cells and astrocytes. Glia 2005; 51:132-147PubMed

32.

Yan H, Lu D, Rivkees SA. Lysophosphatidic acid regulates the proliferation and migration of olfactory ensheathing cells in vitro. Glia 2003; 44:26-36.PubMed

33.

Hatcher H, Planalp R, Cho J, Tortia FM, Torti SV. Curcumin: From ancient medicine to current clinical trials. Cellular and Molecular Life Sci 2008; 65: 1631–1652

34.

Vecchi Brumatti L, Marcuzzi A, Tricarico PM, Zanin V, Girardelli M, Bianco AM. Curcumin and inflammatory bowel disease: potential and limits of innovative treatments. Molecules 2014; 19: 21127-21153.PubMedPubMedCentral

35.

Okudan N, Belviranlı M, Gökbel H, Oz M, Kumak A. Protective effects of curcumin supplementation on intestinal ischemia reperfusion injury. Phytomedicine 2013; 20:844-848PubMed

36.

Cox KH, Pipingas A, Scholey AB. Investigation of the effects of solid lipid curcumin on cognition and mood in a healthy older population. J Psychopharmacol 2015; 29: 642-651PubMed

37.

Kaur H, Patro I, Tikoo K, Sandhir R. Curcumin attenuates inflammatory response and cognitive deficits in experimental model of chronic epilepsy. Neurochem Int 2015; 89:40-50PubMed

38.

Huang TY, Tsai TH, Hsu CW, Hsu YC. Curcuminoids suppress the growth and induce apoptosis through caspase-3-dependent pathways in glioblastoma multiforme (GBM) 8401 cells. J Agric Food Chem 2010; 58:10639-10645.PubMed

39.

Hoppe JB, Coradini K, Frozza RL, et al. Free and nanoencapsulated curcumin suppress β-amyloid-induced cognitive impairments in rats: involvement of BDNF and Akt/GSK-3β signaling pathway. Neurobiol Learn Mem 2013; 106:134-144.PubMed

40.

Pae HO, Jeong SO, Zheng M, et al. Curcumin attenuates ethanol-induced toxicity in HT22 hippocampal cells by activating mitogen-activated protein kinase phosphatase-1. Neurosci Lett 2009; 453: 186–189PubMed

41.

Onder A, Kapan M, Gumus M, et al. The protective effects of curcumin on intestine and remote organs against mesenteric ischemia/reperfusion injury. Turk J Gastroenterol 2012; 23: 141–147PubMed

42.

Mandal MN, Patlolla JM, Zheng L, et al. Curcumin protects retinal cells from light-and oxidant stress-induced cell death. Free Radic Biol Med 2009; 46: 672–679PubMed

43.

Kelsey NA, Wilkins HM, Linseman DA. Nutraceutical antioxidants as novel neuroprotective agents. Molecules 2010; 15:7792-7814.PubMedPubMedCentral

44.

Wang YF, Zu JN, Li J, Chen C, Xi CY, Yan JL. Curcumin promotes the spinal cord repair via inhibition of glial scar formation and inflammation. Neurosci Lett 2014; 560:51-56.PubMed

45.

Tello Velasquez J, Watts ME, Todorovic M, et al. Low-dose curcumin stimulates proliferation, migration and phagocytic activity of olfactory ensheathing cells. PLOS ONE 2014; 9: e111787PubMedPubMedCentral

46.

Kim SJ, Son TG, Park HR, et al. Curcumin stimulates proliferation of embryonic neural progenitor cells and neurogenesis in the adult hippocampus. J Biol Chem 2008; 283: 14497–14505PubMedPubMedCentral

47.

Tello Velasquez J, Nazareth L, Quinn RJ, Ekberg JA, St John JA. Stimulating the proliferation, migration and lamellipodia of Schwann cells using low-dose curcumin. Neuroscience 2016; 2: 324:140-150

48.

Liao KK, Wu MJ, Chen PY, et al. Curcuminoids promote neurite outgrowth in PC12 cells through MAPK/ERK- and PKC-dependent pathways. J Agric Food Chem 2012; 60 :433–443PubMed

49.

Yao M, Yang L, Wang J, et al. Neurological recovery and antioxidant effects of curcumin for spinal cord injury in the rat: a network meta-analysis and systematic review. J Neurotrauma 2015; 32:381-391PubMed

50.

Ramón-Cueto A, Cordero MI, Santos-Benito FF, Avila J. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 2000;25:425-435PubMed

51.

Yang H, Cheng X, Yao Q, Li J, Ju G. The promotive effects of thymosin beta4 on neuronal survival and neurite outgrowth by upregulating L1 expression. Neurochem Res 2008; 33:2269–2280.PubMed

52.

Yang H, Cheng XP, Li JW, Yao Q, Ju G. De-differentiation response of cultured astrocytes to injury induced by scratch or conditioned culture medium of scratch-insulted astrocytes. Cell Mol Neurobiol 2009; 29: 455-473.PubMed

53.

Sergent-Tanguy S, Chagneau C, Neveu I, Naveilhan P. Fluorescent activated cell sorting (FACS): a rapid and reliable method to estimate the number of neurons in a mixed population. J Neurosci Methods 2003; 129:73-79.PubMed

54.

Akimov SS, Belkin AM. Cell surface tissue transglutaminase is involved in adhesion and migration of monocytic cells on fibronectin. Blood 2001;98:1567-1567PubMed

55.

Akimov SS, Belkin AM. Cell-surface transglutaminase promotes fibronectin assembly via interaction with the gelatin-binding domain of fibronectin: a role in TGFbeta-dependent matrix deposition. J Cell Sci 2001; 114:2989-3000.PubMed

56.

Lee J, Kim YS, Choi DH, et al. Transglutaminase-2 induces nuclear factor-kappaB activation via a novel pathway in BV-2 microglia. J Biol Chem 2004; 279:53725-54735PubMed

57.

Kang SK, Lee JY, Chung TW, Kim CH. Overexpression of transglutaminase-2 accelerates the erythroid differentiation of human chronic myelogenous leukemia K562 cell line through PI3K/Akt signaling pathway. FEBS Lett 2004; 577:361-366PubMed

58.

Wang Y, Ande SR, Mishra S. Phosphorylation of transglutaminase 2 (TG2) at serine-216 has a role in TG2 mediated activation of nuclear factor-kappa B and in the downregulation of PTEN. BMC Cancer 2012;12:277PubMedPubMedCentral

59.

Boroughs LK, Antonyak MA, Cerione RA. A novel mechanism by which tissue transglutaminase activates signaling events that promote cell survival. J Biol Chem 2014; 289:10115-10125PubMedPubMedCentral

60.

Almami I, Dickenson JM, Hargreaves AJ, Bonner PL. Modulation of transglutaminase 2 activity in H9c2 cells by PKC and PKA signalling: a role for transglutaminase 2 in cytoprotection.Br J Pharmacol 2014; 171:3946-3960.PubMedPubMedCentral

61.

Eckert RL, Kaartinen MT, Nurminskaya M, et al. Transglutaminase regulation of cell function. Physiol Rev 2014; 94:383-417.PubMedPubMedCentral

62.

Fadok VA, Bratton DL, Rose DM, Pearson A, Ezekewitz RA, Henson PM. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature. 2000; 405: 85-90.PubMed

63.

Li MO, Sarkisian MR, Mehal WZ, Rakic P, Flavell RA. Phosphatidylserine receptor is required for clearance of apoptotic cells. Science 2003;302:1560-1563PubMed

64.

Wong K, Valdez PA, Tan C, Yeh S, Hongo JA, Ouyang W. Phosphatidylserine receptor Tim-4 is essential for the maintenance of the homeostatic state of resident peritoneal macrophages. Proc Natl Acad Sci U S A 2010;107:8712-8717PubMedPubMedCentral

65.

Yang H, Chen YZ , Zhang Y, et al. A lysine-rich motif in the phosphatidylserine receptor PSR-1 mediates recognition and removal of apoptotic cells. Nat Commun 2015; 6:5717PubMedPubMedCentral

66.

Lee IH, Bulte JW, Schweinhardt P, et al. In vivo magnetic resonance tracking of olfactory ensheathing glia grafted into the rat spinal cord. Exp Neurol 2004;187:509-516PubMed

67.

Barnett SC, Riddell JS. Olfactory ensheathing cell transplantation as a strategy for spinal cord repair—what can it achieve? Nat Clin Pract Neurol 2007; 3:152-161.PubMed

68.

Vincent AJ, Choi-Lundberg DL, Harris JA, West AK, Chuah MI. Bacteria and PAMPs activate nuclear factor kappaB and Gro production in a subset of olfactory ensheathing cells and astrocytes but not in Schwann cells. Glia 2007; 55:905-916.PubMed

69.

Hassler SN, Johnson KM, Hulsebosch CE. Reactive oxygen species and lipid peroxidation inhibitors reduce mechanical sensitivity in a chronic neuropathic pain model of spinal cord injury in rats. J Neurochem 2014; 131:413-417.PubMedPubMedCentral

70.

Cooney SJ, Zhao Y, Byrnes KR. Characterization of the expression and inflammatory activity of NADPH oxidase after spinal cord injury. Free Radic Res 2014; 48:929-939PubMedPubMedCentral

71.

Siegel M, Khosia C. Transglutaminase 2 inhibitors and their therapeutic role in disease states. Pharmacol Ther 2007; 115:232-245PubMedPubMedCentral

72.

Tong L, Png E, Aihua H, et al. Molecular mechanism of transglutaminase-2 in corneal epithelial migration and adhesion. Biochim Biophys Acta 2013;1833:1304-1315

73.

Janiak A, Zemskov EA, Belkin M. Cell surface transglutaminase promotes RhoA activation via integrin clustering and suppression of the Src-p190RhoGAP signaling pathway. Mol Biol Cell 2006; 17:1606-1619PubMedPubMedCentral

74.

Vandivier RW, Fadok VA, Hoffmann PR, et al. Elastase-mediated phosphatidylserine receptor cleavage impairs apoptotic cell clearance in cystic fibrosis and bronchiectasis. J Clin Invest 2002; 109: 661-670PubMedPubMedCentral

Title: Lipopolysaccharide and Curcumin Co-Stimulation Potentiates Olfactory Ensheathing Cell Phagocytosis Via Enhancing Their Activation
Authors: Ding-Jun Hao
Cuicui Liu
Lingling Zhang
Bo Chen
Qian Zhang
Rui Zhang
Jing An
Jingjing Zhao
Mingmei Wu
Yi Wang
Alfred Simental
Baorong He
Hao Yang
Publication date: 01-04-2017
Publisher: Springer International Publishing
Published in: Neurotherapeutics / Issue 2/2017
Print ISSN: 1933-7213
Electronic ISSN: 1878-7479
DOI: https://doi.org/10.1007/s13311-016-0485-8

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Lipopolysaccharide and Curcumin Co-Stimulation Potentiates Olfactory Ensheathing Cell Phagocytosis Via Enhancing Their Activation

Abstract

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Springer Medicine

Abstract

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