Exosomes Derived from Mesenchymal Stromal Cells Promote Axonal Growth of Cortical Neurons

Molecular Neurobiology

Volumn 54, Issue 4, 2017, Pages 2659-2673

  Zhang, Yi ^a   Chopp, Michael ^a,b   Liu, Xian Shuang ^a   Katakowski, Mark ^a   Wang, Xinli ^a   Tian, Xinchu ^c   Wu, David ^c   Zhang, Zheng Gang ^a  

^a HENRY FORD HOSPITAL   (United States)

^b OAKLAND UNIVERSITY   (United States)

^c Troy High School   (United States)

Author keywords

Axon; Exosomes; Mesenchymal stromal cells; MicroRNA

Indexed keywords

ARGONAUTE 2 PROTEIN; BOTULINUM TOXIN; MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA; MICRORNA 17 92; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEOCHONDROITIN SULFATE; SNARE PROTEIN; UNCLASSIFIED DRUG; AGO2 PROTEIN, RAT; ARGONAUTE PROTEIN;

ANIMAL CELL; ARTICLE; BRAIN CELL; CONTROLLED STUDY; EMBRYO; EXOSOME; INTERNALIZATION; MESENCHYMAL STROMA CELL; MICROFLUIDICS; NEURITE OUTGROWTH; NONHUMAN; PERIKARYON; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; AXON; DRUG EFFECTS; ENDOCYTOSIS; GENETICS; METABOLISM; WISTAR RAT;

ANIMALS; ARGONAUTE PROTEINS; AXONS; BOTULINUM TOXINS; CHONDROITIN SULFATE PROTEOGLYCANS; ENDOCYTOSIS; EXOSOMES; MESENCHYMAL STROMAL CELLS; MICRORNAS; RATS, WISTAR; SIGNAL TRANSDUCTION; SNARE PROTEINS;

EID: 84961218139     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-016-9851-0     Document Type: Article

References (77)

1. Horner PJ, Gage FH (2000) Regenerating the damaged central nervous system. Nature 407(6807):963–970. doi:10.1038/35039559
2. Chen MS, Huber AB, van der Haar ME, Frank M, Schnell L, Spillmann AA, Christ F, Schwab ME (2000) Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403(6768):434–439. doi:10.1038/35000219
3. Morgenstern DA, Asher RA, Fawcett JW (2002) Chondroitin sulphate proteoglycans in the CNS injury response. Prog Brain Res 137:313–332
4. Ueno Y, Chopp M, Zhang L, Buller B, Liu Z, Lehman NL, Liu XS, Zhang Y et al (2012) Axonal outgrowth and dendritic plasticity in the cortical peri-infarct area after experimental stroke. Stroke 43(8):2221–2228. doi:10.1161/STROKEAHA.111.646224
5. Chaudhry N, Filbin MT (2007) Myelin-associated inhibitory signaling and strategies to overcome inhibition. J Cereb Blood Flow Metab 27(6):1096–1107. doi:10.1038/sj.jcbfm.9600407
6. Fitch MT, Silver J (2008) CNS injury, glial scars, and inflammation: inhibitory extracellular matrices and regeneration failure. Exp Neurol 209(2):294–301. doi:10.1016/j.expneurol.2007.05.014
7. Singh P, Yan J, Hull R, Read S, O’Sullivan J, Henderson RD, Rose S, Greer JM et al (2011) Levels of phosphorylated axonal neurofilament subunit H (pNfH) are increased in acute ischemic stroke. J Neurol Sci 304(1–2):117–121. doi:10.1016/j.jns.2011.01.025
8. Snyder EY, Yoon C, Flax JD, Macklis JD (1997) Multipotent neural precursors can differentiate toward replacement of neurons undergoing targeted apoptotic degeneration in adult mouse neocortex. Proc Natl Acad Sci U S A 94(21):11663–11668
9. Brustle O, Jones KN, Learish RD, Karram K, Choudhary K, Wiestler OD, Duncan ID, McKay RD (1999) Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science 285(5428):754–756
10. Stichel CC, Muller HW (1998) Experimental strategies to promote axonal regeneration after traumatic central nervous system injury. Prog Neurobiol 56(2):119–148
11. Ayaz D, Leyssen M, Koch M, Yan J, Srahna M, Sheeba V, Fogle KJ, Holmes TC et al (2008) Axonal injury and regeneration in the adult brain of Drosophila. J Neurosci 28(23):6010–6021. doi:10.1523/JNEUROSCI.0101-08.2008
12. Liu Z, Chopp M, Ding X, Cui Y, Li Y (2013) Axonal remodeling of the corticospinal tract in the spinal cord contributes to voluntary motor recovery after stroke in adult mice. Stroke 44(7):1951–1956. doi:10.1161/STROKEAHA.113.001162
13. Hancock ML, Preitner N, Quan J, Flanagan JG (2014) MicroRNA-132 is enriched in developing axons, locally regulates Rasa1 mRNA, and promotes axon extension. J Neurosci 34(1):66–78. doi:10.1523/JNEUROSCI.3371-13.2014
14. Sasaki Y, Gross C, Xing L, Goshima Y, Bassell GJ (2014) Identification of axon-enriched microRNAs localized to growth cones of cortical neurons. Dev Neurobiol 74(3):397–406. doi:10.1002/dneu.22113
15. Kim HH, Kim P, Phay M, Yoo S (2015) Identification of precursor microRNAs within distal axons of sensory neuron. J Neurochem 134(2):193–199. doi:10.1111/jnc.13140
16. Zhang Y, Ueno Y, Liu XS, Buller B, Wang X, Chopp M, Zhang ZG (2013) The MicroRNA-17-92 cluster enhances axonal outgrowth in embryonic cortical neurons. J Neurosci 33(16):6885–6894. doi:10.1523/JNEUROSCI.5180-12.2013
17. Zhang Y, Chopp M, Liu X, Kassis H, Wang X, Li C, An G, Gang Zhang Z (2015) MicroRNAs in the axon locally mediate the effects of chondroitin sulfate proteoglycans and cGMP on axonal growth. Dev Neurobiol. doi:10.1002/dneu.22292
18. Fevrier B, Raposo G (2004) Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr Opin Cell Biol 16(4):415–421. doi:10.1016/j.ceb.2004.06.003
19. Raposo G, Stoorvogel W (2013) Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 200(4):373–383. doi:10.1083/jcb.201211138
20. Braicu C, Tomuleasa C, Monroig P, Cucuianu A, Berindan-Neagoe I, Calin GA (2015) Exosomes as divine messengers: are they the Hermes of modern molecular oncology? Cell Death Differ 22(1):34–45. doi:10.1038/cdd.2014.130
21. Xin H, Li Y, Liu Z, Wang X, Shang X, Cui Y, Zhang ZG, Chopp M (2013) MiR-133b promotes neural plasticity and functional recovery after treatment of stroke with multipotent mesenchymal stromal cells in rats via transfer of exosome-enriched extracellular particles. Stem Cells 31(12):2737–2746. doi:10.1002/stem.1409
22. Xin H, Li Y, Cui Y, Yang JJ, Zhang ZG, Chopp M (2013) Systemic administration of exosomes released from mesenchymal stromal cells promote functional recovery and neurovascular plasticity after stroke in rats. J Cereb Blood Flow Metab 33(11):1711–1715. doi:10.1038/jcbfm.2013.152
23. Zhang Y, Chopp M, Meng Y, Katakowski M, Xin H, Mahmood A, Xiong Y (2015) Effect of exosomes derived from multipluripotent mesenchymal stromal cells on functional recovery and neurovascular plasticity in rats after traumatic brain injury. J Neurosurg 122(4):856–867. doi:10.3171/2014.11.JNS14770
24. Xin H, Li Y, Buller B, Katakowski M, Zhang Y, Wang X, Shang X, Zhang ZG et al (2012) Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth. Stem Cells 30(7):1556–1564. doi:10.1002/stem.1129
25. Taylor AM, Rhee SW, Tu CH, Cribbs DH, Cotman CW, Jeon NL (2003) Microfluidic multicompartment device for neuroscience research. Langmuir 19(5):1551–1556. doi:10.1021/la026417v
26. Taylor AM, Blurton-Jones M, Rhee SW, Cribbs DH, Cotman CW, Jeon NL (2005) A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat Methods 2(8):599
27. Brewer GJ, Torricelli JR (2007) Isolation and culture of adult neurons and neurospheres. Nat Protoc 2(6):1490–1498. doi:10.1038/nprot.2007.207
28. Xu SY, Wu YM, Ji Z, Gao XY, Pan SY (2012) A modified technique for culturing primary fetal rat cortical neurons. J Biomed Biotechnol 2012:803930. doi:10.1155/2012/803930
29. Zhang RL, Chopp M, Gregg SR, Toh Y, Roberts C, Letourneau Y, Buller B, Jia L et al (2009) Patterns and dynamics of subventricular zone neuroblast migration in the ischemic striatum of the adult mouse. J Cereb Blood Flow Metab 29(7):1240–1250. doi:10.1038/jcbfm.2009.55
30. Guduric-Fuchs J, O’Connor A, Camp B, O’Neill CL, Medina RJ, Simpson DA (2012) Selective extracellular vesicle-mediated export of an overlapping set of microRNAs from multiple cell types. BMC Genomics 13:357. doi:10.1186/1471-2164-13-357
31. Melo SA, Sugimoto H, O’Connell JT, Kato N, Villanueva A, Vidal A, Qiu L, Vitkin E et al (2014) Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis. Cancer Cell 26(5):707–721. doi:10.1016/j.ccell.2014.09.005
32. Pecho-Vrieseling E, Rieker C, Fuchs S, Bleckmann D, Esposito MS, Botta P, Goldstein C, Bernhard M et al (2014) Transneuronal propagation of mutant huntingtin contributes to non-cell autonomous pathology in neurons. Nat Neurosci 17(8):1064–1072. doi:10.1038/nn.3761
33. Sudhof TC, Rizo J (2011) Synaptic vesicle exocytosis. Cold Spring Harb Perspect Biol 3 (12). doi:10.1101/cshperspect.a005637
34. Gracias NG, Shirkey-Son NJ, Hengst U (2014) Local translation of TC10 is required for membrane expansion during axon outgrowth. Nat Commun 5:3506. doi:10.1038/ncomms4506
35. Liu XS, Chopp M, Zhang RL, Hozeska-Solgot A, Gregg SC, Buller B, Lu M, Zhang ZG (2009) Angiopoietin 2 mediates the differentiation and migration of neural progenitor cells in the subventricular zone after stroke. J Biol Chem 284(34):22680–22689. doi:10.1074/jbc.M109.006551
36. Meijering E, Jacob M, Sarria JC, Steiner P, Hirling H, Unser M (2004) Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58(2):167–176. doi:10.1002/cyto.a.20022
37. Andreassi C, Zimmermann C, Mitter R, Fusco S, Devita S, Saiardi A, Riccio A (2010) An NGF-responsive element targets myo-inositol monophosphatase-1 mRNA to sympathetic neuron axons. Nat Neurosci 13(3):291–301. doi:10.1038/nn.2486
38. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25(4):402–408. doi:10.1006/meth.2001.1262
39. Zhang Z, Wang D, Sun T, Xu J, Chiang HC, Shin W, Wu LG (2013) The SNARE proteins SNAP25 and synaptobrevin are involved in endocytosis at hippocampal synapses. J Neurosci 33(21):9169–9175. doi:10.1523/JNEUROSCI.0301-13.2013
40. Chen S, Hall C, Barbieri JT (2008) Substrate recognition of VAMP-2 by botulinum neurotoxin B and tetanus neurotoxin. J Biol Chem 283(30):21153–21159. doi:10.1074/jbc.M800611200
41. Peng L, Liu H, Ruan H, Tepp WH, Stoothoff WH, Brown RH, Johnson EA, Yao WD et al (2013) Cytotoxicity of botulinum neurotoxins reveals a direct role of syntaxin 1 and SNAP-25 in neuron survival. Nat Commun 4:1472. doi:10.1038/ncomms2462
42. Koga Y, Yasunaga M, Moriya Y, Akasu T, Fujita S, Yamamoto S, Matsumura Y (2011) Exosome can prevent RNase from degrading microRNA in feces. J Gastrointest Oncol 2(4):215–222. doi:10.3978/j.issn.2078-6891.2011.015
43. Macfarlane LA, Murphy PR (2010) MicroRNA: biogenesis, function and role in cancer. Curr Genomics 11(7):537–561. doi:10.2174/138920210793175895
44. Meister G (2013) Argonaute proteins: functional insights and emerging roles. Nat Rev Genet 14(7):447–459. doi:10.1038/nrg3462
45. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O (2009) Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 11(9):1143–1149. doi:10.1038/ncb1929
46. Yiu G, He Z (2006) Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 7(8):617–627. doi:10.1038/nrn1956
47. Toy D, Namgung U (2013) Role of glial cells in axonal regeneration. Exp Neurobiol 22(2):68–76. doi:10.5607/en.2013.22.2.68
48. Filbin MT (2003) Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci 4(9):703–713. doi:10.1038/nrn1195
49. Haas CA, Rauch U, Thon N, Merten T, Deller T (1999) Entorhinal cortex lesion in adult rats induces the expression of the neuronal chondroitin sulfate proteoglycan neurocan in reactive astrocytes. J Neurosci 19(22):9953–9963
50. Xiong Y, Mahmood A, Chopp M (2010) Angiogenesis, neurogenesis and brain recovery of function following injury. Curr Opin Investig Drugs 11(3):298–308
51. Zhang ZG, Chopp M (2009) Neurorestorative therapies for stroke: underlying mechanisms and translation to the clinic. Lancet Neurol 8(5):491–500. doi:10.1016/S1474-4422(09)70061-4
52. Li Y, Chopp M (2009) Marrow stromal cell transplantation in stroke and traumatic brain injury. Neurosci Lett 456(3):120–123. doi:10.1016/j.neulet.2008.03.096
53. Chopp M, Li Y (2002) Treatment of neural injury with marrow stromal cells. Lancet Neurol 1(2):92–100
54. Chopp M, Li Y, Zhang J (2008) Plasticity and remodeling of brain. J Neurol Sci 265(1–2):97–101. doi:10.1016/j.jns.2007.06.013
55. Fruhbeis C, Frohlich D, Kuo WP, Amphornrat J, Thilemann S, Saab AS, Kirchhoff F, Mobius W et al (2013) Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte-neuron communication. PLoS Biol 11(7), e1001604. doi:10.1371/journal.pbio.1001604
56. Lopez-Verrilli MA, Picou F, Court FA (2013) Schwann cell-derived exosomes enhance axonal regeneration in the peripheral nervous system. Glia 61(11):1795–1806. doi:10.1002/glia.22558
57. Ha M, Kim VN (2014) Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 15(8):509–524. doi:10.1038/nrm3838
58. Winter J, Diederichs S (2011) Argonaute proteins regulate microRNA stability: increased microRNA abundance by Argonaute proteins is due to microRNA stabilization. RNA Biol 8(6):1149–1157. doi:10.4161/rna.8.6.17665
59. Aschrafi A, Schwechter AD, Mameza MG, Natera-Naranjo O, Gioio AE, Kaplan BB (2008) MicroRNA-338 regulates local cytochrome c oxidase IV mRNA levels and oxidative phosphorylation in the axons of sympathetic neurons. J Neurosci 28(47):12581–12590. doi:10.1523/JNEUROSCI.3338-08.2008
60. Dajas-Bailador F, Bonev B, Garcez P, Stanley P, Guillemot F, Papalopulu N (2012) microRNA-9 regulates axon extension and branching by targeting Map1b in mouse cortical neurons. Nat Neurosci 15(5):697–699. doi:10.1038/nn.3082
61. Lu CS, Zhai B, Mauss A, Landgraf M, Gygi S, Van Vactor D (2014) MicroRNA-8 promotes robust motor axon targeting by coordinate regulation of cell adhesion molecules during synapse development. Philos Trans R Soc Lond B Biol Sci 369 (1652). doi:10.1098/rstb.2013.0517
62. Park KK, Liu K, Hu Y, Smith PD, Wang C, Cai B, Xu B, Connolly L et al (2008) Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 322(5903):963–966. doi:10.1126/science.1161566
63. He Z (2010) Intrinsic control of axon regeneration. J Biomed Res 24(1):2–5. doi:10.1016/S1674-8301(10)60002-4
64. Gardner RT, Habecker BA (2013) Infarct-derived chondroitin sulfate proteoglycans prevent sympathetic reinnervation after cardiac ischemia-reperfusion injury. J Neurosci 33(17):7175–7183. doi:10.1523/JNEUROSCI.5866-12.2013
65. Xu B, Park D, Ohtake Y, Li H, Hayat U, Liu J, Selzer ME, Longo FM et al (2015) Role of CSPG receptor LAR phosphatase in restricting axon regeneration after CNS injury. Neurobiol Dis 73:36–48. doi:10.1016/j.nbd.2014.08.030
66. Vuppalanchi D, Willis DE, Twiss JL (2009) Regulation of mRNA transport and translation in axons. Results Probl Cell Differ 48:193–224. doi:10.1007/400_2009_16
67. Yoo S, van Niekerk EA, Merianda TT, Twiss JL (2010) Dynamics of axonal mRNA transport and implications for peripheral nerve regeneration. Exp Neurol 223(1):19–27. doi:10.1016/j.expneurol.2009.08.011
68. Willis DE, Twiss JL (2011) Profiling axonal mRNA transport. Methods Mol Biol 714:335–352. doi:10.1007/978-1-61779-005-8_21
69. Mulcahy LA, Pink RC, Carter DR (2014) Routes and mechanisms of extracellular vesicle uptake. J Extracellular Vesicles 3. doi:10.3402/jev.v3.24641
70. Corrado C, Raimondo S, Chiesi A, Ciccia F, De Leo G, Alessandro R (2013) Exosomes as intercellular signaling organelles involved in health and disease: basic science and clinical applications. Int J Mol Sci 14(3):5338–5366. doi:10.3390/ijms14035338
71. Tian T, Zhu YL, Zhou YY, Liang GF, Wang YY, Hu FH, Xiao ZD (2014) Exosome uptake through clathrin-mediated endocytosis and macropinocytosis and mediating miR-21 delivery. J Biol Chem 289(32):22258–22267. doi:10.1074/jbc.M114.588046
72. Svensson KJ, Christianson HC, Wittrup A, Bourseau-Guilmain E, Lindqvist E, Svensson LM, Morgelin M, Belting M (2013) Exosome uptake depends on ERK1/2-heat shock protein 27 signaling and lipid Raft-mediated endocytosis negatively regulated by caveolin-1. J Biol Chem 288(24):17713–17724. doi:10.1074/jbc.M112.445403
73. Valapala M, Vishwanatha JK (2011) Lipid raft endocytosis and exosomal transport facilitate extracellular trafficking of annexin A2. J Biol Chem 286(35):30911–30925. doi:10.1074/jbc.M111.271155
74. Fitzner D, Schnaars M, van Rossum D, Krishnamoorthy G, Dibaj P, Bakhti M, Regen T, Hanisch UK et al (2011) Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis. J Cell Sci 124(Pt 3):447–458. doi:10.1242/jcs.074088
75. Escrevente C, Keller S, Altevogt P, Costa J (2011) Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer 11:108. doi:10.1186/1471-2407-11-108
76. Goda Y (1997) SNAREs and regulated vesicle exocytosis. Proc Natl Acad Sci U S A 94(3):769–772
77. Xu J, Luo F, Zhang Z, Xue L, Wu XS, Chiang HC, Shin W, Wu LG (2013) SNARE proteins synaptobrevin, SNAP-25, and syntaxin are involved in rapid and slow endocytosis at synapses. Cell Rep 3(5):1414–1421. doi:10.1016/j.celrep.2013.03.010