Exosomes as a novel pathway for regulating development and diseases of the skin (Review)

  • Authors:
    • Ying Liu
    • Haidong Wang
    • Juan Wang
  • View Affiliations

  • Published online on: January 31, 2018     https://doi.org/10.3892/br.2018.1054
  • Pages: 207-214
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
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Abstract

Exosomes are one of the most potent intercellular communicators, which are able to communicate with adjacent or distant cells. Exosomes deliver various bioactive molecules, including membrane receptors, proteins, mRNA and microRNA, to target cells and serve roles. Recent studies have demonstrated that exosomes may regulate the functions and diseases of the skin, which is the largest organ of the human body. The abnormal functions of the skin lead to the progression of scleroderma, melanoma, baldness and other diseases. A previous study has demonstrated that epithelial progenitor cells are rich in several subunits of exosomes that may maintain the proliferative capacity of these epithelial progenitor cells, which is essential for the development of the epidermis. Exosomes derived from human adipose mesenchymal stem cells accelerate skin wound healing by optimizing fibroblast properties; this is beneficial for the recovery of postoperative and other wounds. Exosomes derived from adipocytes promote melanoma migration and invasion through fatty acid oxidation; therefore, in the clinic, it may be possible to improve the prognosis of patients with melanoma by reducing their body fat content. Exosomes derived from keratinocytes modulate melanocyte pigmentation, which has been utilized as a novel mechanism for the regulation of pigmentation in conditions including Moynahan syndrome and albinism. Meanwhile, scleroderma patients with vascular abnormalities may experience decreased serum exosome levels; it may therefore be possible to detect the exosome content in sera in order to diagnose and treat scleroderma. In addition, the use of exosomes has been suggested to promote or enhance hair growth, which has been demonstrated to be highly effective. These studies have provided new opportunities and therapeutic strategies for understanding how exosomes regulate intercellular communication in pathological processes of the skin.

References

1 

Ng KW and Lau WM: Skin Deep: The Basics of Human Skin Structure and Drug Penetration. Springer-Verlag; Berlin Heidelberg, New York: 2015

2 

Menon GK: Skin basics; structure and functionLipids and Skin Health. Springer International Publishing; Switzerland: pp. 9–23. 2015

3 

Barbieri JS, Wanat K and Seykora J: Skin: Basic structure and functionPathobiology of Human Disease. Academic Press; pp. 1134–1144. 2014, View Article : Google Scholar

4 

Mcgrath JA, Eady RAJ and Pope FM: Anatomy and organization of human skinRook's Textbook of Dermatology. 7th. Wiley; pp. 45–128. 2008

5 

Hay RJ, Johns NE, Williams HC, Bolliger IW, Dellavalle RP, Margolis DJ, Marks R, Naldi L, Weinstock MA, Wulf SK, et al: The global burden of skin disease in 2010: An analysis of the prevalence and impact of skin conditions. J Invest Dermatol. 134:1527–1534. 2014. View Article : Google Scholar : PubMed/NCBI

6 

Lo Cicero A, Delevoye C, Gilles-Marsens F, Loew D, Dingli F, Guéré C, André N, Vié K, van Niel G and Raposo G: Exosomes released by keratinocytes modulate melanocyte pigmentation. Nat Commun. 6:75062015. View Article : Google Scholar : PubMed/NCBI

7 

Felicetti F, De Feo A, Coscia C, Puglisi R, Pedini F, Pasquini L, Bellenghi M, Errico MC, Pagani E and Carè A: Exosome-mediated transfer of miR-222 is sufficient to increase tumor malignancy in melanoma. J Transl Med. 14:562016. View Article : Google Scholar : PubMed/NCBI

8 

Lin J, Li J, Huang B, Liu J, Chen X, Chen XM, Xu YM, Huang LF and Wang XZ: Exosomes: Novel biomarkers for clinical diagnosis. Sci World J. 2015:6570862015. View Article : Google Scholar

9 

Properzi F, Logozzi M and Fais S: Exosomes: The future of biomarkers in medicine. Biomarkers Med. 7:769–778. 2013. View Article : Google Scholar

10 

Cocucci E, Racchetti G and Meldolesi J: Shedding microvesicles: Artefacts no more. Trends Cell Biol. 19:43–51. 2009. View Article : Google Scholar : PubMed/NCBI

11 

Bach DH, Hong JY, Park HJ and Lee SK: The role of exosomes and miRNAs in drug-resistance of cancer cells. Int J Cancer. 141:220–230. 2017. View Article : Google Scholar : PubMed/NCBI

12 

Lai RC, Chen TS and Lim SK: Mesenchymal stem cell exosome: A novel stem cell-based therapy for cardiovascular disease. Regen Med. 6:481–492. 2011. View Article : Google Scholar : PubMed/NCBI

13 

Rabinowits G, Gerçel-Taylor C, Day JM, Taylor DD and Kloecker GH: Exosomal microRNA: A diagnostic marker for lung cancer. Clin Lung Cancer. 10:42–46. 2009. View Article : Google Scholar : PubMed/NCBI

14 

Yan Y, Jiang W, Tan Y, Zou S, Zhang H, Mao F, Gong A, Qian H and Xu W: hucMSC exosome-derived GPX1 is required for the recovery of hepatic oxidant injury. Mol Ther. 25:465–479. 2017. View Article : Google Scholar : PubMed/NCBI

15 

Li J, Chen Y, Guo X, Zhou L, Jia Z, Peng Z, Tang Y, Liu W, Zhu B, Wang L and Ren C: GPC1 exosome and its regulatory miRNAs are specific markers for the detection and target therapy of colorectal cancer. J Cell Mol Med. 21:838–847. 2017. View Article : Google Scholar : PubMed/NCBI

16 

Proksch E, Brandner JM and Jensen JM: The skin: An indispensable barrier. Exp Dermatol. 17:1063–1072. 2008. View Article : Google Scholar : PubMed/NCBI

17 

Forslind B and Lindberg M: Skin, Hair, and Nails: Structure and Function. CRC Press; 2003

18 

Bang C, Batkai S, Dangwal S, Gupta SK, Foinquinos A, Holzmann A, Just A, Remke J, Zimmer K, Zeug A, et al: Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J Clin Invest. 124:2136–2146. 2014. View Article : Google Scholar : PubMed/NCBI

19 

Holmes D: Adipose tissue: Adipocyte exosomes drive melanoma progression. Nat Rev Endocrinol. 12:4362016. View Article : Google Scholar

20 

Bickers DR and Athar M: Oxidative stress in the pathogenesis of skin disease. J Invest Dermatol. 126:2565–2575. 2006. View Article : Google Scholar : PubMed/NCBI

21 

Akita N, Sawamura D, Matsumura K and Nomura K: Clinical study of diflorasone diacetate ointment (Diflal® ointment) in various types of skin diseases. Skin Res. 29:115–119. 2010.

22 

Balato N, Megna M, Ayala F, Balato A, Napolitano M and Patruno C: Effects of climate changes on skin diseases. Expert Rev Anti Infect Ther. 12:171–181. 2014. View Article : Google Scholar : PubMed/NCBI

23 

Liu L, Song P, Yi X, Li C and Gao T: 067 Serum-derived exosomes contribute to abnormal melanocyte function in patients with active vitiligo. J Invest Dermatol. 136:S12. 2016. View Article : Google Scholar

24 

Hu L, Wang J, Zhou X, Xiong Z, Zhao J, Yu R, Huang F, Zhang H and Chen L: Exosomes derived from human adipose mensenchymal stem cells accelerates cutaneous wound healing via optimizing the characteristics of fibroblasts. Sci Rep. 6:329932016. View Article : Google Scholar : PubMed/NCBI

25 

Goedert L, Koya R, Hu-Lieskovan S and Ribas A: Exosomes as a predictor tool of acquired resistance to melanoma treatment. BMC Proc. 8 Suppl 4:pp. P282014; View Article : Google Scholar

26 

Xiao D, Barry S, Kmetz D, Egger M, Pan J, Rai SN, Qu J, McMasters KM and Hao H: Melanoma cell-derived exosomes promote epithelial-mesenchymal transition in primary melanocytes through paracrine/autocrine signaling in the tumor microenvironment. Cancer Lett. 376:318–327. 2016. View Article : Google Scholar : PubMed/NCBI

27 

Simpson RJ, Jensen SS and Lim JW: Proteomic profiling of exosomes: Current perspectives. Proteomics. 8:4083–4099. 2008. View Article : Google Scholar : PubMed/NCBI

28 

Vlassov AV, Magdaleno S, Setterquist R and Conrad R: Exosomes: Current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim Biophys Acta. 1820:940–948. 2012. View Article : Google Scholar : PubMed/NCBI

29 

Pan BT and Johnstone RM: Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: Selective externalization of the receptor. Cell. 33:967–978. 1983. View Article : Google Scholar : PubMed/NCBI

30 

Mathivanan S, Ji H and Simpson RJ: Exosomes: Extracellular organelles important in intercellular communication. J Proteomics. 73:1907–1920. 2010. View Article : Google Scholar : PubMed/NCBI

31 

Simpson RJ, Lim JW, Moritz RL and Mathivanan S: Exosomes: Proteomic insights and diagnostic potential. Expert Rev Proteomics. 6:267–283. 2009. View Article : Google Scholar : PubMed/NCBI

32 

Lakkaraju A and Rodriguez-Boulan E: Itinerant exosomes: Emerging roles in cell and tissue polarity. Trends Cell Biol. 18:199–209. 2008. View Article : Google Scholar : PubMed/NCBI

33 

van Niel G, Porto-Carreiro I, Simoes S and Raposo G: Exosomes: A common pathway for a specialized function. J Biochem. 140:13–21. 2006. View Article : Google Scholar : PubMed/NCBI

34 

Segura MF, Hanniford D, Menendez S, Reavie L, Zou X, Alvarez-Diaz S, Zakrzewski J, Blochin E, Rose A, Bogunovic D, et al: Aberrant miR-182 expression promotes melanoma metastasis by repressing FOXO3 and microphthalmia-associated transcription factor. Proc Natl Acad Sci USA. 106:pp. 1814–1819. 2009; View Article : Google Scholar : PubMed/NCBI

35 

Conde-Vancells J, Rodriguez-Suarez E, Embade N, Gil D, Matthiesen R, Valle M, Elortza F, Lu SC, Mato JM and Falcon-Perez JM: Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes. J Proteome Res. 7:5157–5166. 2008. View Article : Google Scholar : PubMed/NCBI

36 

Zhou H, Cheruvanky A, Hu X, Matsumoto T, Hiramatsu N, Cho ME, Berger A, Leelahavanichkul A, Doi K, Chawla LS, et al: Urinary exosomal transcription factors, a new class of biomarkers for renal disease. Kidney Int. 74:613–621. 2008. View Article : Google Scholar : PubMed/NCBI

37 

Théry C, Ostrowski M and Segura E: Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 9:581–593. 2009. View Article : Google Scholar : PubMed/NCBI

38 

Ichim T and Bogin V: Therapeutic immune modulation by stem cell secreted exosomes. US Patent 20160361399 A1. August 4–2016.issued December 15, 2016.

39 

Liu Q, Rojas-Canales DM, Divito SJ, Shufesky WJ, Stolz DB, Erdos G, Sullivan ML, Gibson GA, Watkins SC, Larregina AT, et al: Donor dendritic cell-derived exosomes promote allograft-targeting immune response. J Clin Invest. 126:2805–2820. 2016. View Article : Google Scholar : PubMed/NCBI

40 

Zhao H, Yang L, Baddour J, Achreja A, Bernard V, Moss T, Marini JC, Tudawe T, Seviour EG, San Lucas FA, et al: Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism. Elife. 5:e102502016. View Article : Google Scholar : PubMed/NCBI

41 

Yi H, Ye J, Yang XM, Zhang LW, Zhang ZG and Chen YP: High-grade ovarian cancer secreting effective exosomes in tumor angiogenesis. Int J Clin Exp Pathol. 8:5062–5070. 2015.PubMed/NCBI

42 

Tickner JA, Urquhart AJ, Stephenson SA, Richard DJ and O'Byrne KJ: Functions and therapeutic roles of exosomes in cancer. Front Oncol. 4:1272014. View Article : Google Scholar : PubMed/NCBI

43 

Saleem SN and Abdel-Mageed AB: Tumor-derived exosomes in oncogenic reprogramming and cancer progression. Cell Mol Life Sci. 72:1–10. 2015. View Article : Google Scholar : PubMed/NCBI

44 

Chevillet JR, Kang Q, Ruf IK, Briggs HA, Vojtech LN, Hughes SM, Cheng HH, Arroyo JD, Meredith EK, Gallichotte EN, et al: Quantitative and stoichiometric analysis of the microRNA content of exosomes. Proc Natl Acad Sci USA. 111:pp. 14888–14893. 2014; View Article : Google Scholar : PubMed/NCBI

45 

Bi S, Wang C, Jin Y, Lv Z, Xing X and Lu Q: Correlation between serum exosome derived miR-208a and acute coronary syndrome. Int J Clin Exp Med. 8:4275–4280. 2015.PubMed/NCBI

46 

Wang H and Wang B: Extracellular vesicle microRNAs mediate skeletal muscle myogenesis and disease. Biomed Rep. 5:296–300. 2016. View Article : Google Scholar : PubMed/NCBI

47 

Humphries B: Dissecting the mechanism by which microRNA-200b inhibits breast cancer metastasis. PhD dissertationMichigan State University 2016

48 

Wang B, Yao K, Huuskes BM, Shen HH, Zhuang J, Godson C, Brennan EP, Wilkinson-Berka JL, Wise AF and Ricardo SD: Mesenchymal stem cells deliver exogenous microRNA-let7c via exosomes to attenuate renal fibrosis. Mol Ther. 24:1290–1301. 2016. View Article : Google Scholar : PubMed/NCBI

49 

Lou G, Song X, Yang F, Wu S, Wang J, Chen Z and Liu Y: Exosomes derived from miR-122-modified adipose tissue-derived MSCs increase chemosensitivity of hepatocellular carcinoma. J Hematol Oncol. 8:1222015. View Article : Google Scholar : PubMed/NCBI

50 

Ji Q, Ji Y, Peng J, Zhou X, Chen X, Zhao H, Xu T, Chen L and Xu Y: Increased brain-specific miR-9 and miR-124 in the serum exosomes of acute ischemic stroke patients. PLoS One. 11:e01636452016. View Article : Google Scholar : PubMed/NCBI

51 

Jackson SJ, Zhang Z, Feng D, Flagg M, O'Loughlin E, Wang D, Stokes N, Fuchs E and Yi R: Rapid and widespread suppression of self-renewal by microRNA-203 during epidermal differentiation. Development. 140:1882–1891. 2013. View Article : Google Scholar : PubMed/NCBI

52 

Nijhof JG, van Pelt C, Mulder AA, Mitchell DL, Mullenders LH and de Gruijl FR: Epidermal stem and progenitor cells in murine epidermis accumulate UV damage despite NER proficiency. Carcinogenesis. 28:792–800. 2007. View Article : Google Scholar : PubMed/NCBI

53 

Mistry DS, Chen Y and Sen GL: Progenitor function in self-renewing human epidermis is maintained by the exosome. Cell Stem Cell. 11:127–135. 2012. View Article : Google Scholar : PubMed/NCBI

54 

Noiret M, Mottier S, Angrand G, Gautier-Courteille C, Lerivray H, Viet J, Paillard L, Mereau A, Hardy S and Audic Y: Ptbp1 and Exosc9 knockdowns trigger skin stability defects through different pathways. Dev Biol. 409:489–501. 2016. View Article : Google Scholar : PubMed/NCBI

55 

Clevers H: Wnt/β-catenin signaling in development and disease. Cell. 127:469–480. 2006. View Article : Google Scholar : PubMed/NCBI

56 

Gross JC, Chaudhary V, Bartscherer K and Boutros M: Active Wnt proteins are secreted on exosomes. Nat Cell Biol. 14:1036–1045. 2012. View Article : Google Scholar : PubMed/NCBI

57 

Zhang B, Wang M, Gong A, Zhang X, Wu X, Zhu Y, Shi H, Wu L, Zhu W, Qian H and Xu W: HucMSC-exosome mediated-Wnt4 signaling is required for cutaneous wound healing. Stem Cells. 33:2158–2168. 2015. View Article : Google Scholar : PubMed/NCBI

58 

Varothai S and Bergfeld WF: Androgenetic alopecia: An evidence-based treatment update. Am J Clin Dermatol. 15:217–230. 2014. View Article : Google Scholar : PubMed/NCBI

59 

Lim SK, Yeo MSW, Chen TS and Lai RC: Use of exosomes to promote or enhance hair growth EP Patent 2629782 A1. October 17–2011, issued August 28, 2013.

60 

Lin JY and Fisher DE: Melanocyte biology and skin pigmentation. Nature. 445:843–850. 2007. View Article : Google Scholar : PubMed/NCBI

61 

Rawlings AV: Ethnic skin types: Are there differences in skin structure and function? Int J Cosmet Sci. 28:79–93. 2006. View Article : Google Scholar : PubMed/NCBI

62 

Whitton M, Pinart M, Batchelor JM, Leonardi-Bee J, Gonzalez U, Jiyad Z, Eleftheriadou V and Ezzedine K: Evidence-based management of vitiligo: Summary of a Cochrane systematic review. Br J Dermatol. 174:962–969. 2016. View Article : Google Scholar : PubMed/NCBI

63 

Zhang J, Guan J, Niu X, Hu G, Guo S, Li Q, Xie Z, Zhang C and Wang Y: Exosomes released from human induced pluripotent stem cells-derived MSCs facilitate cutaneous wound healing by promoting collagen synthesis and angiogenesis. J Transl Med. 13:492015. View Article : Google Scholar : PubMed/NCBI

64 

Li X, Jiang C and Zhao J: Human endothelial progenitor cells-derived exosomes accelerate cutaneous wound healing in diabetic rats by promoting endothelial function. J Diabetes Complications. 30:986–992. 2016. View Article : Google Scholar : PubMed/NCBI

65 

Gallet R, Dawkins J, Valle J, Simsolo E, de Couto G, Middleton R, Tseliou E, Luthringer D, Kreke M, Smith RR, et al: Exosomes secreted by cardiosphere-derived cells reduce scarring, attenuate adverse remodelling, and improve function in acute and chronic porcine myocardial infarction. Eur Heart J. 38:201–211. 2017.PubMed/NCBI

66 

Zhao B, Zhang Y, Han S, Zhang W, Zhou Q, Guan H, Liu J, Shi J, Su L and Hu D: Exosomes derived from human amniotic epithelial cells accelerate wound healing and inhibit scar formation. J Mol Histol. 48:121–132. 2017. View Article : Google Scholar : PubMed/NCBI

67 

Zhang B, Wu X, Zhang X, Sun Y, Yan Y, Shi H, Zhu Y, Wu L, Pan Z, Zhu W, et al: Human umbilical cord mesenchymal stem cell exosomes enhance angiogenesis through the Wnt4/β-catenin pathway. Stem Cells Transl Med. 4:513–522. 2015. View Article : Google Scholar : PubMed/NCBI

68 

Nakamura K, Jinnin M, Fukushima S and Ihn H: Exosome expression in the skin and sera of systemic sclerosis patients, and its possible therapeutic application against skin ulcer. J Dermatol Sci. 84:e97–e98. 2016. View Article : Google Scholar

69 

Diepgen TL and Mahler V: The epidemiology of skin cancer. Br J Dermatol. 146 Suppl 61:1–6. 2002. View Article : Google Scholar : PubMed/NCBI

70 

Wernli KJ, Henrikson NB, Morrison CC, Nguyen M, Pocobelli G and Blasi PR: Screening for skin cancer in adults: Updated evidence report and systematic review for the US Preventive Services Task Force. JAMA. 316:436–447. 2016. View Article : Google Scholar : PubMed/NCBI

71 

Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, et al: Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 363:711–723. 2010. View Article : Google Scholar : PubMed/NCBI

72 

Alegre E, Zubiri L, Perez-Gracia JL, González-Cao M, Soria L, Martín-Algarra S and González A: Circulating melanoma exosomes as diagnostic and prognosis biomarkers. Clin Chim Acta. 454:28–32. 2016. View Article : Google Scholar : PubMed/NCBI

73 

Gray-Schopfer V, Wellbrock C and Marais R: Melanoma biology and new targeted therapy. Nature. 445:851–857. 2007. View Article : Google Scholar : PubMed/NCBI

74 

Gajos-Michniewicz A, Duechler M and Czyz M: miRNA in melanoma-derived exosomes. Cancer Lett. 347:29–37. 2014. View Article : Google Scholar : PubMed/NCBI

75 

Hood JL, San RS and Wickline SA: Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res. 71:3792–3801. 2011. View Article : Google Scholar : PubMed/NCBI

76 

Ekström EJ, Bergenfelz C, von Bülow V, Serifler F, Carlemalm E, Jönsson G, Andersson T and Leandersson K: WNT5A induces release of exosomes containing pro-angiogenic and immunosuppressive factors from malignant melanoma cells. Mol Cancer. 13:882014. View Article : Google Scholar : PubMed/NCBI

77 

Hood JL: Melanoma exosomes enable tumor tolerance in lymph nodes. Med Hypotheses. 90:11–13. 2016. View Article : Google Scholar : PubMed/NCBI

78 

Shoshan E, Mobley AK, Braeuer RR, Kamiya T, Huang L, Vasquez ME, Salameh A, Lee HJ, Kim SJ, Ivan C, et al: Reduced adenosine-to-inosine miR-455-5p editing promotes melanoma growth and metastasis. Nat Cell Biol. 17:311–321. 2015. View Article : Google Scholar : PubMed/NCBI

79 

Zhou J, Xu D, Xie H, Tang J, Liu R, Li J, Wang S, Chen X, Su J, Zhou X, et al: miR-33a functions as a tumor suppressor in melanoma by targeting HIF-1α. Cancer Biol Ther. 16:846–855. 2015. View Article : Google Scholar : PubMed/NCBI

80 

Bhattacharya A, Schmitz U, Raatz Y, Schönherr M, Kottek T, Schauer M, Franz S, Saalbach A, Anderegg U, Wolkenhauer O, et al: miR-638 promotes melanoma metastasis and protects melanoma cells from apoptosis and autophagy. Oncotarget. 6:2966–2980. 2015. View Article : Google Scholar : PubMed/NCBI

81 

Alegre E, Sanmamed MF, Rodriguez C, Carranza O, Martín-Algarra S and González A: Study of circulating microRNA-125b levels in serum exosomes in advanced melanoma. Arch Pathol Lab Med. 138:828–832. 2014. View Article : Google Scholar : PubMed/NCBI

82 

Pfeffer SR, Grossmann KF, Cassidy PB, Yang CH, Fan M, Kopelovich L, Leachman SA and Pfeffer LM: Detection of exosomal miRNAs in the plasma of melanoma patients. J Clin Med. 4:2012–2027. 2015. View Article : Google Scholar : PubMed/NCBI

83 

Mutschelknaus L, Peters C, Winkler K, Yentrapalli R, Heider T, Atkinson MJ and Moertl S: Exosomes derived from squamous head and neck cancer promote cell survival after ionizing radiation. PLoS One. 11:e01522132016. View Article : Google Scholar : PubMed/NCBI

84 

Languino LR, Singh A, Prisco M, Inman GJ, Luginbuhl A, Curry JM and South AP: Exosome-mediated transfer from the tumor microenvironment increases TGFβ signaling in squamous cell carcinoma. Am J Transl Res. 8:2432–2437. 2016.PubMed/NCBI

85 

Jelonek K, Wojakowska A, Marczak L, Muer A, Tinhofer-Keilholz I, Lysek-Gladysinska M, Widlak P and Pietrowska M: Ionizing radiation affects protein composition of exosomes secreted in vitro from head and neck squamous cell carcinoma. Acta Biochim Pol. 62:265–272. 2015. View Article : Google Scholar : PubMed/NCBI

86 

Toki S, Motegi S, Yamada K, Uchiyama A, Kanai S, Yamanaka M and Ishikawa O: Clinical and laboratory features of systemic sclerosis complicated with localized scleroderma. J Dermatol. 42:283–287. 2015. View Article : Google Scholar : PubMed/NCBI

87 

Nakamura K, Jinnin M, Harada M, Kudo H, Nakayama W, Inoue K, Ogata A, Kajihara I, Fukushima S and Ihn H: Altered expression of CD63 and exosomes in scleroderma dermal fibroblasts. J Dermatol Sci. 84:30–39. 2016. View Article : Google Scholar : PubMed/NCBI

88 

Brouwer R, Pruijn GJ and van Venrooij WJ: The human exosome: An autoantigenic complex of exoribonucleases in myositis and scleroderma. Arthritis Res. 3:102–106. 2001. View Article : Google Scholar : PubMed/NCBI

89 

Gutiérrez-Ramos R, Gonz Lez-Díaz V, Pacheco-Tovar MG, López-Luna A, Avalos-Díaz E and Herrera-Esparza R: A dermatomyositis and scleroderma overlap syndrome with a remarkable high titer of anti-exosome antibodies. Reumatismo. 60:296–300. 2008.PubMed/NCBI

90 

Barkai L and Paragh G: Metabolic syndrome in childhood and adolescence. Orv Hetil. 147:243–250. 2006.(In Hungarian). PubMed/NCBI

91 

Rajala MW and Scherer PE: Minireview: The adipocyte - at the crossroads of energy homeostasis, inflammation, and atherosclerosis. Endocrinology. 144:3765–3773. 2003. View Article : Google Scholar : PubMed/NCBI

92 

Ferrante SC, Nadler EP, Pillai DK, Hubal MJ, Wang Z, Wang JM, Gordish-Dressman H, Koeck E, Sevilla S, Wiles AA and Freishtat RJ: Adipocyte-derived exosomal miRNAs: A novel mechanism for obesity-related disease. Pediatr Res. 77:447–454. 2015. View Article : Google Scholar : PubMed/NCBI

93 

Zhang Y, Yu M, Dai M, Chen C, Tang Q, Jing W, Wang H and Tian W: miR-450a-5p within rat adipose tissue exosome-like vesicles promotes adipogenic differentiation by targeting WISP2. J Cell Sci. 130:1158–1168. 2017.PubMed/NCBI

94 

Skowron F, Bérard F, Balme B and Maucort-Boulch D: Role of obesity on the thickness of primary cutaneous melanoma. J Eur Acad Dermatol Venereol. 29:262–269. 2015. View Article : Google Scholar : PubMed/NCBI

95 

Lazar I, Clement E, Dauvillier S, Milhas D, Ducoux-Petit M, LeGonidec S, Moro C, Soldan V, Dalle S, Balor S, et al: Adipocyte exosomes promote melanoma aggressiveness through fatty acid oxidation: a novel mechanism linking obesity and cancer. Cancer Res. 76:4051–4057. 2016. View Article : Google Scholar : PubMed/NCBI

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APA
Liu, Y., Wang, H., & Wang, J. (2018). Exosomes as a novel pathway for regulating development and diseases of the skin (Review). Biomedical Reports, 8, 207-214. https://doi.org/10.3892/br.2018.1054
MLA
Liu, Y., Wang, H., Wang, J."Exosomes as a novel pathway for regulating development and diseases of the skin (Review)". Biomedical Reports 8.3 (2018): 207-214.
Chicago
Liu, Y., Wang, H., Wang, J."Exosomes as a novel pathway for regulating development and diseases of the skin (Review)". Biomedical Reports 8, no. 3 (2018): 207-214. https://doi.org/10.3892/br.2018.1054