HucMSC Exosome-Delivered 14-3-3ζ Orchestrates Self-Control of the Wnt Response via Modulation of YAP During Cutaneous Regeneration

Stem Cells

Volumn 34, Issue 10, 2016, Pages 2485-2500

  Zhang, Bin ^a   Shi, Yinghong ^a   Gong, Aihua ^a   Pan, Zhaoji ^a   Shi, Hui ^a   Yang, Huan ^a   Fu, Hailong ^a   Yan, Yongmin ^a   Zhang, Xu ^a   Wang, Mei ^a   Zhu, Wei ^a   Qian, Hui ^a   Xu, Wenrong ^a,b  

^a Ningbo Addiction Research and Treatment Center   (China)

^b JIANGSU UNIVERSITY   (China)

Author keywords

14 3 3 protein; Cutaneous regeneration; Exosomes; Stem cells; Wnt; YAP

Indexed keywords

BETA CATENIN; CELL PROTEIN; COLLAGEN; PROTEIN 14 3 3; PROTEIN 14 3 3ZETA; PROTEIN YAP; SERINE; UNCLASSIFIED DRUG; WNT PROTEIN; WNT4 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BURN; CELL DENSITY; COMPLEX FORMATION; CONTROLLED STUDY; CUTANEOUS REGENERATION; EXOSOME; HUMAN; HUMAN CELL; HUMAN TISSUE; HUMAN UMBILICAL CORD MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; PROTEOMICS; RAT; SIGNAL TRANSDUCTION; STEM CELL EXPANSION; TISSUE REGENERATION; TISSUE REPAIR;

EID: 84990855885     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2432     Document Type: Article

References (54)

1. Bielefeld KA, Amini-Nik S Alman BA. Cutaneous wound healing: Recruiting developmental pathways for regeneration. Cell Mol Life Sci 2013;70:2059–2081.
2. Martin P. Wound healing–aiming for perfect skin regeneration. Science 1997;276:75–81.
3. Singer AJ, Clark RA. Cutaneous wound healing. N Engl J Med 1999;341:738–746.
4. Vermeulen L. Keeping stem cells in check: a hippo balancing act. Cell Stem Cell 2013;12:3–5.
5. Depaepe V, Suarez-Gonzalez N, Dufour A et al. Ephrin signalling controls brain size by regulating apoptosis of neural progenitors. Nature 2005;435:1244–1250.
6. Kim KA, Kakitani M, Zhao J et al. Mitogenic influence of human R-spondin1 on the intestinal epithelium. Science 2005;309:1256–1259.
7. Stanger BZ, Datar R, Murtaugh LC et al. Direct regulation of intestinal fate by Notch. Proc Natl Acad Sci USA 2005;102:12443–12448.
8. Schorey JS, Bhatnagar S. Exosome function: From tumor immunology to pathogen biology. Traffic 2008;9:871–881.
9. Bruno S, Grange C, Deregibus MC et al. Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J Am Soc Nephrol 2009;20:1053–1067.
10. Gatti S, Bruno S, Deregibus MC et al. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrol Dial Transplant 2011;26:1474–1483.
11. Li L, Jin S, Zhang Y. Ischemic preconditioning potentiates the protective effect of mesenchymal stem cells on endotoxin-induced acute lung injury in mice through secretion of exosome. Int J Clin Exp Med 2015;8:3825–3832.
12. Xin H, Li Y, Buller B et al. Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth. Stem Cells 2012;30:1556–1564.
13. Zhou Y, Xu H, Xu W et al. Exosomes released by human umbilical cord mesenchymal stem cells protect against cisplatin-induced renal oxidative stress and apoptosis in vivo and in vitro. Stem Cell Res Ther 2013;4:34.
14. Li T, Yan Y, Wang B et al. Exosomes derived from human umbilical cord mesenchymal stem cells alleviate liver fibrosis. Stem Cells Dev 2013;22:845–854.
15. Gross JC, Chaudhary V, Bartscherer K et al. Active wnt proteins are secreted on exosomes. Nat Cell Biol 2012;14:1036–1045.
16. Zhang B, Wang M, Gong A et al. HucMSC-exosome Mediated-Wnt4 signaling is required for cutaneous wound Healing. Stem Cells 2015;33:2158–2168.
17. Zhang B, Wu X, Zhang X et al. Human umbilical cord mesenchymal stem cell exosomes enhance angiogenesis through the Wnt4/beta-catenin pathway. Stem Cells Transl Med 2015;4:513–522.
18. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006;127:469–480.
19. Distler A, Deloch L, Huang J et al. Inactivation of tankyrases reduces experimental fibrosis by inhibiting canonical Wnt signalling. Ann Rheum Dis 2013;72:1575–1580.
20. DiRocco DP, Kobayashi A, Taketo MM et al. Wnt4/beta-catenin signaling in medullary kidney myofibroblasts. J Am Soc Nephrol 2013;24:1399–1412.
21. Edgar BA. From cell structure to transcription: Hippo forges a new path. Cell 2006;124:267–273.
22. Harvey K, Tapon N. The Salvador-Warts-hippo pathway—an emerging tumour-suppressor network. Nat Rev Cancer 2007;7:182–191.
23. Pan D. The hippo signaling pathway in development and cancer. Dev Cell 2010;19:491–505.
24. Zhao B, Li L, Guan KL. Hippo signaling at a glance. J Cell Sci 2010;123:4001–4006.
25. Varelas X. The hippo pathway effectors TAZ and YAP in development, homeostasis and disease. Development 2014;141:1614–1626.
26. Dong J, Feldmann G, Huang J et al. Elucidation of a universal size-control mechanism in drosophila and mammals. Cell 2007;130:1120–1133.
27. Reddy BV, Rauskolb C, Irvine KD. Influence of fat-hippo and notch signaling on the proliferation and differentiation of drosophila optic neuroepithelia. Development 2010;137:2397–2408.
28. Zhang H, Pasolli HA, Fuchs E. Yes-associated protein (YAP) transcriptional coactivator functions in balancing growth and differentiation in skin. Proc Natl Acad Sci U S A 2011;108:2270–2275.
29. Barry ER, Morikawa T, Butler BL et al. Restriction of intestinal stem cell expansion and the regenerative response by YAP. Nature 2013;493:106–110.
30. Qiao C, Xu W, Zhu W et al. Human mesenchymal stem cells isolated from the umbilical cord. Cell Biol Int 2008;32:8–15.
31. Nakamura Y, Ishikawa H, Kawai K et al. Enhanced wound healing by topical administration of mesenchymal stem cells transfected with stromal cell-derived factor-1. Biomaterials 2013;34:9393–9400.
32. Baht GS, Silkstone D, Vi L et al. Exposure to a youthful circulation rejuvenates bone repair through modulation of beta-catenin. Nat Commun 2015;6:7131.
33. Brack AS, Conboy MJ, Roy S et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 2007;317:807–810.
34. Zhao B, Wei X, Li W et al. Inactivation of YAP oncoprotein by the hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 2007;21:2747–2761.
35. Drees F, Pokutta S, Yamada S et al. Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell 2005;123:903–915.
36. Schlegelmilch K, Mohseni M, Kirak O et al. Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 2011;144:782–795.
37. Azzolin L, Panciera T, Soligo S et al. YAP/TAZ incorporation in the beta-catenin destruction complex orchestrates the wnt response. Cell 2014;158:157–170.
38. Feng Y, Irvine KD. Fat and expanded act in parallel to regulate growth through warts. Proc Natl Acad Sci U S A 2007;104:20362–20367.
39. Lei QY, Zhang H, Zhao B et al. TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the hippo pathway. Mol Cell Biol 2008;28:2426–2436.
40. Jerome M, Paudel HK. 14-3-3zeta regulates nuclear trafficking of protein phosphatase 1alpha (PP1alpha) in HEK-293 cells. Arch Biochem Biophys 2014;558:28–35.
41. 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.
42. Kolf CM, Song L, Helm J et al. Nascent osteoblast matrix inhibits osteogenesis of human mesenchymal stem cells in vitro. Stem Cell Res Ther 2015;6:258.
43. Etheridge SL, Spencer GJ, Heath DJ et al. Expression profiling and functional analysis of wnt signaling mechanisms in mesenchymal stem cells. Stem Cells 2004;22:849–860.
44. Zhou S. Paracrine effects of haematopoietic cells on human mesenchymal stem cells. Sci Rep 2015;5:10573.
45. Mesa KR, Rompolas P, Zito G et al. Niche-induced cell death and epithelial phagocytosis regulate hair follicle stem cell pool. Nature 2015;522:94–97.
46. Clevers H, Loh KM, Nusse R. Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science 2014;346:1248012.
47. Blanpain C. Stem cells: Skin regeneration and repair. Nature 2010;464:686–687.
48. Varelas X, Miller BW, Sopko R et al. The hippo pathway regulates wnt/beta-catenin signaling. Dev Cell 2010;18:579–591.
49. Imajo M, Miyatake K, Iimura A et al. A molecular mechanism that links hippo signalling to the inhibition of wnt/beta-catenin signalling. EMBO J 2012;31:1109–1122.
50. Azzolin L, Zanconato F, Bresolin S et al. Role of TAZ as mediator of Wnt signaling. Cell 2012;151:1443–1456.
51. Ford JC, Al-Khodairy F, Fotou E et al. 14-3-3 Protein homologs required for the DNA damage checkpoint in fission yeast. Science 1994;265:533–535.
52. Fu H, Subramanian RR, Masters SC. 14-3-3 Proteins: Structure, function, and regulation. Annu Rev Pharmacol Toxicol 2000;40:617–647.
53. Xing H, Zhang S, Weinheimer C et al. 14-3-3 Proteins block apoptosis and differentially regulate MAPK cascades. EMBO J 2000;19:349–358.
54. Chimen M, McGettrick HM, Apta B et al. Homeostatic regulation of T cell trafficking by a B cell-derived peptide is impaired in autoimmune and chronic inflammatory disease. Nat Med 2015;21:467–475.