Grape exosome-like nanoparticles induce intestinal stem cells and protect mice from DSS-induced colitis

Molecular Therapy

Volumn 21, Issue 7, 2013, Pages 1345-1357

  Ju, Songwen ^b   Mu, Jingyao ^b   Dokland, Terje ^c   Zhuang, Xiaoying ^b   Wang, Qilong ^b   Jiang, Hong ^b   Xiang, Xiaoyu ^b   Deng, Zhong Bin ^b   Wang, Baomei ^b   Zhang, Lifeng ^b   Roth, Mary ^e   Welti, Ruth ^e   Mobley, James ^d   Jun, Yan ^b   Miller, Donald ^b   Zhang, Huang Ge ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b University of Louisville School of Medicine   (United States)

^c University of Alabama at Birmingham   (United States)

^d University of Alabama at Birmingham   (United States)

^e KANSAS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; DEXTRAN SULFATE; GRAPE EXOSOME NANOPARTICLE; NANOPARTICLE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; COCULTURE; COLITIS; CONTROLLED STUDY; EXOSOME; GRAPE; INTESTINAL STEM CELL; LIPIDOMICS; MOUSE; NONHUMAN; STEM CELL; WNT SIGNALING PATHWAY;

MUS; VITACEAE;

EID: 84879686252     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.64     Document Type: Article

References (48)

1. Johnstone, RM, Adam, M, Hammond, JR, Orr, L and Turbide, C (1987). Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 262: 9412-9420.
2. Wolfers, J, Lozier, A, Raposo, G, Regnault, A, Théry, C, Masurier, C et al. (2001). Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 7: 297-303. (Pubitemid 32224344)
3. Valadi, H, Ekström, K, Bossios, A, Sjöstrand, M, Lee, JJ and Lötvall, JO (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659. (Pubitemid 47214727)
4. Zhang, HG, Liu, C, Su, K, Su, K, Yu, S, Zhang, L et al. (2006). A membrane form of TNF-alpha presented by exosomes delays T cell activation-induced cell death. J Immunol 176: 7385-7393. (Pubitemid 43849040)
5. Liu, C, Yu, S, Zinn, K, Wang, J, Zhang, L, Jia, Y et al. (2006). Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function. J Immunol 176: 1375-1385. (Pubitemid 43134279)
6. Théry, C, Ostrowski, M and Segura, E (2009). Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9: 581-593.
7. An, Q, Hückelhoven, R, Kogel, KH and van Bel, AJ (2006). Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus. Cell Microbiol 8: 1009-1019. (Pubitemid 43675331)
8. Regente, M, Pinedo, M, Elizalde, M and de la Canal, L (2012). Apoplastic exosome-like vesicles: a new way of protein secretion in plants? Plant Signal Behav 7: 544-546.
9. Nielsen, ME, Feechan, A, Böhlenius, H, Ueda, T and Thordal-Christensen, H (2012). Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. Proc Natl Acad Sci USA 109: 11443-11448.
10. Wei, T, Hibino, H and Omura, T (2009). Release of Rice dwarf virus from insect vector cells involves secretory exosomes derived from multivesicular bodies. Commun Integr Biol 2: 324-326.
11. Xiang, X, Liu, Y, Zhuang, X, Zhang, S, Michalek, S, Taylor, DD et al. (2010). TLR2-mediated expansion of MDSCs is dependent on the source of tumor exosomes. Am J Pathol 177: 1606-1610.
12. Guo, L, Mishra, G, Markham, JE, Li, M, Tawfall, A, Welti, R et al. (2012). Connections between sphingosine kinase and phospholipase D in the abscisic acid signaling pathway in Arabidopsis. J Biol Chem 287: 8286-8296.
13. Peters, C, Li, M, Narasimhan, R, Roth, M, Welti, R and Wang, X (2010). Nonspecifc phospholipase C NPC4 promotes responses to abscisic acid and tolerance to hyperosmotic stress in Arabidopsis. Plant Cell 22: 2642-2659.
14. Wang, YY, Lai, SK, So, C, Schneider, C, Cone, R and Hanes, J (2011). Mucoadhesive nanoparticles may disrupt the protective human mucus barrier by altering its microstructure. PLoS ONE 6: e21547.
15. Cone, RA (2009). Barrier properties of mucus. Adv Drug Deliv Rev 61: 75-85.
16. Lai, SK, Suk, JS, Pace, A, Wang, YY, Yang, M, Mert, O et al. (2011). Drug carrier nanoparticles that penetrate human chronic rhinosinusitis mucus. Biomaterials 32: 6285-6290.
17. Lai, SK, Wang, YY and Hanes, J (2009). Mucus-penetrating nanoparticles for drug and gene delivery to mucosal tissues. Adv Drug Deliv Rev 61: 158-171.
18. Zhuang, X, Xiang, X, Grizzle, W, Sun, D, Zhang, S, Axtell, RC et al. (2011). Treatment of brain infammatory diseases by delivering exosome encapsulated anti-infammatory drugs from the nasal region to the brain. Mol Ther 19: 1769-1779.
19. Huss, M, Ingenhorst, G, König, S, Gassel, M, Dröse, S, Zeeck, A et al. (2002). Concanamycin A, the specifc inhibitor of V-ATPases, binds to the V(o) subunit c. J Biol Chem 277: 40544-40548. (Pubitemid 35215633)
20. Niikura, K (2006). Vacuolar ATPase as a drug discovery target. Drug News Perspect 19: 139-144. (Pubitemid 43886095)
21. Sato, T, Vries, RG, Snippert, HJ, van de Wetering, M, Barker, N, Stange, DE et al. (2009). Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459: 262-265.
22. Naro, F, Donchenko, V, Minotti, S, Zolla, L, Molinaro, M and Adamo, S (1997). Role of phospholipase C and D signalling pathways in vasopressin-dependent myogenic differentiation. J Cell Physiol 171: 34-42. (Pubitemid 27158326)
23. Grange, M, Sette, C, Cuomo, M, Conti, M, Lagarde, M, Prigent, AF et al. (2000). The cAMP-specifc phosphodiesterase PDE4D3 is regulated by phosphatidic acid binding. Consequences for cAMP signaling pathway and characterization of a phosphatidic acid binding site. J Biol Chem 275: 33379-33387.
24. van Es, JH, Haegebarth, A, Kujala, P, Itzkovitz, S, Koo, BK, Boj, SF et al. (2012). A critical role for the Wnt effector Tcf4 in adult intestinal homeostatic self-renewal. Mol Cell Biol 32: 1918-1927.
25. Kim, TH, Escudero, S and Shivdasani, RA (2012). Intact function of Lgr5 receptor-expressing intestinal stem cells in the absence of Paneth cells. Proc Natl Acad Sci USA 109: 3932-3937.
26. Fauser, JK, Donato, R P, Woenig, JA, Proctor, SJ, Trotta, AP, Grover, PK et al. (2012). Wnt blockade with dickkopf reduces intestinal crypt fssion and intestinal growth in infant rats. J Pediatr Gastroenterol Nutr 55: 26-31.
27. Yan, KS, Chia, LA, Li, X, Ootani, A, Su, J, Lee, JY et al. (2012). The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations. Proc Natl Acad Sci USA 109: 466-471.
28. Birchmeier, W (2011). Stem cells: Orphan receptors fnd a home. Nature 476: 287-288.
29. de Lau, W, Barker, N, Low, TY, Koo, BK, Li, VS, Teunissen, H et al. (2011). Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling. Nature 476: 293-297.
30. Marsh, V, Winton, DJ, Williams, GT, Dubois, N, Trumpp, A, Sansom, OJ et al. (2008). Epithelial Pten is dispensable for intestinal homeostasis but suppresses adenoma development and progression after Apc mutation. Nat Genet 40: 1436-1444.
31. Jiang, S, Bailey, AS, Goldman, DC, Swain, JR, Wong, MH, Streeter, PR et al. (2008). Hematopoietic stem cells contribute to lymphatic endothelium. PLoS ONE 3: e3812.
32. de la Roche, M, Rutherford, TJ, Gupta, D, Veprintsev, DB, Saxty, B, Freund, SM et al. (2012). An intrinsically labile alpha-helix abutting the BCL9-binding site of beta-catenin is required for its inhibition by carnosic acid. Nat Commun 3: 680.
33. Itzkovitz, S, Lyubimova, A, Blat, IC, Maynard, M, van Es, J, Lees, J et al. (2012). Singlemolecule transcript counting of stem-cell markers in the mouse intestine. Nat Cell Biol 14: 106-114.
34. Zeki, SS, Graham, TA and Wright, NA (2011). Stem cells and their implications for colorectal cancer. Nat Rev Gastroenterol Hepatol 8: 90-100.
35. Snippert, HJ, van der Flier, LG, Sato, T, van Es, JH, van den Born, M, Kroon-Veenboer, C et al. (2010). Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143: 134-144.
36. Barker, N, Huch, M, Kujala, P, van de Wetering, M, Snippert, HJ, van Es, JH et al. (2010). Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 6: 25-36.
37. van der Flier, LG, van Gijn, ME, Hatzis, P, Kujala, P, Haegebarth, A, Stange, DE et al. (2009). Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell 136: 903-912.
38. Cheasley, D, Pereira, L, Lightowler, S, Vincan, E, Malaterre, J and Ramsay, RG (2011). Myb controls intestinal stem cell genes and self-renewal. Stem Cells 29: 2042-2050.
39. Shin, K, Lee, J, Guo, N, Kim, J, Lim, A, Qu, L et al. (2011). Hedgehog/Wnt feedback supports regenerative proliferation of epithelial stem cells in bladder. Nature 472: 110-114.
40. Takashima, S, Kadowaki, M, Aoyama, K, Koyama, M, Oshima, T, Tomizuka, K et al. (2011). The Wnt agonist R-spondin1 regulates systemic graft-versus-host disease by protecting intestinal stem cells. J Exp Med 208: 285-294.
41. Spence, JR, Mayhew, CN, Rankin, SA, Kuhar, MF, Vallance, JE, Tolle, K et al. (2011). Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 470: 105-109.
42. Sato, T, van Es, JH, Snippert, HJ, Stange, DE, Vries, RG, van den Born, M et al. (2011). Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469: 415-418.
43. Spilman, MS, Welbon, C, Nelson, E and Dokland, T (2009). Cryo-electron tomography of porcine reproductive and respiratory syndrome virus: organization of the nucleocapsid. J Gen Virol 90(Pt 3): 527-535.
44. Xiao, S, Gao, W, Chen, QF, Chan, SW, Zheng, SX, Ma, J et al. (2010). Overexpression of Arabidopsis acyl-CoA binding protein ACBP3 promotes starvation-induced and age-dependent leaf senescence. Plant Cell 22: 1463-1482.
45. Laulagnier, K, Motta, C, Hamdi, S, Roy, S, Fauvelle, F, Pageaux, JF et al. (2004). Mast cell-and dendritic cell-derived exosomes display a specifc lipid composition and an unusual membrane organization. Biochem J 380(Pt 1): 161-171. (Pubitemid 38725741)
46. Bligh, EG and Dyer, WJ (1959). A rapid method of total lipid extraction and purifcation. Can J Biochem Physiol 37: 911-917.
47. Wang, GJ, Liu, Y, Qin, A, Shah, SV, Deng, ZB, Xiang, X et al. (2008). Thymus exosomes-like particles induce regulatory T cells. J Immunol 181: 5242-5248.
48. Liu, Y, Xiang, X, Zhuang, X, Zhang, S, Liu, C, Cheng, Z et al. (2010). Contribution of MyD88 to the tumor exosome-mediated induction of myeloid derived suppressor cells. Am J Pathol 176: 2490-2499.