Ultraviolet B preconditioning enhances the hair growth-promoting effects of adipose-derived stem cells via generation of reactive oxygen species

Stem Cells and Development

Volumn 22, Issue 1, 2013, Pages 158-168

  Jeong, Yun Mi ^a,b   Sung, Young Kwan ^c   Kim, Wang Kyun ^a,b   Kim, Ji Hye ^a,b   Kwack, Mi Hee ^c   Yoon, Insoo ^d   Kim, Dae Duk ^d   Sung, Jong Hyuk ^a,b  

^a CHA University   (South Korea)

^b CHA Stem Cell Institute   (South Korea)

^c Kyungpook National University School of Medicine   (South Korea)

^d Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DIPHENYLIODONIUM SALT; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SMALL INTERFERING RNA;

ADIPOSE DERIVED STEM CELL; ANGIOGENESIS; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; FLOW CYTOMETRY; HAIR GROWTH; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIATION DOSE; STEM CELL TRANSPLANTATION; ULTRAVIOLET B RADIATION; WESTERN BLOTTING;

ADULT STEM CELLS; ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; ENZYME INDUCTION; FEMALE; HAIR; HAIR FOLLICLE; HUMANS; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, NUDE; NADPH OXIDASE; PARACRINE COMMUNICATION; REACTIVE OXYGEN SPECIES; REGENERATION; STEM CELL TRANSPLANTATION; SUBCUTANEOUS FAT; ULTRAVIOLET RAYS;

MUS;

EID: 84871438689     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2012.0167     Document Type: Article

References (43)

1. Wei X, Z Du, L Zhao, D Feng, G Wei, Y He, J Tan, WH Lee, H Hampel, et al. (2009). IFATS collection: the conditioned media of adipose stromal cells protect against hypoxiaischemia- induced brain damage in neonatal rats. Stem Cells 27:478-488.
2. Kondo K, S Shintani, R Shibata, H Murakami, R Murakami, M Imaizumi, Y Kitagawa and T Murohara. (2009). Implantation of adipose-derived regenerative cells enhances ischemia-induced angiogenesis. Arterioscler Thromb Vasc Biol 29:61-66.
3. Rehman J, D Traktuev, J Li, S Merfeld-Clauss, CJ Temm- Grove, JE Bovenkerk, CL Pell, BH Johnstone, RV Considine and KL March. (2004). Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 109:1292-1298. (Pubitemid 38372789)
4. Song SY, HM Chung and JH Sung. (2010). The pivotal role ofVEGF in adipose-derived-stem-cell-mediated regeneration. Expert Opin Biol Ther 10:1529-1537.
5. Chung HM, CH Won and JH Sung. (2009). Responses of adipose-derived stem cells during hypoxia: enhanced skin-regenerative potential. Expert Opin Biol Ther 9: 1499-1508.
6. Lee EY, Y Xia, WS Kim, MH Kim, TH Kim, KJ Kim, BS Parkand JH Sung. (2009). Hypoxia-enhanced wound-healing function of adipose-derived stem cells: increase in stem cell proliferation and up-regulation of VEGF and bFGF. Wound Repair Regen 17:540-547.
7. Kim JH, SH Park, SG Park, JS Choi, Y Xia and JH Sung. (2011).The pivotal role of reactive oxygen species generation in the hypoxia-induced stimulation of adipose-derived stem cells. Stem Cells Dev 20:1753-1761.
8. Kim JH, SY Song, SK Park, SU Song, Y Xia and JH Sung. (2012). Primary involvement of NADPH oxidase 4 in hypoxia- induced generation of reactive oxygen species in adipose- derived stem cells. Stem Cells Dev. [Epub ahead of print]; DOI:10.1089/scd.2011.0561.
9. Won CH, HG Yoo, OS Kwon, MY Sung, YJ Kang, JH Chung, BS Park, JH Sung, WS Kim and KH Kim. (2010). Hair growth promoting effects of adipose tissue-derived stem cells. J Dermatol Sci 57:134-137.
10. Lee MJ, J Kim, MY Kim, YS Bae, SH Ryu, TG Lee and JH Kim. (2010). Proteomic analysis of tumor necrosis factor-alpha- induced secretome of human adipose tissue-derived mesenchymal stem cells. J Proteome Res 9:1754-1762.
11. Grant WB. (2008). The effect of solar UVB doses and vitamin D production, skin cancer action spectra, and smoking in explaining links between skin cancers and solid tumours. Eur J Cancer 44:12-15. (Pubitemid 350262831)
12. Osmancevic A, K Landin-Wilhelmsen, O Larko, D Mellstrom, AM Wennberg, L Hulthen and AL Krogstad. (2007). UVB therapy increases 25(OH) vitamin D syntheses in postmenopausal women with psoriasis. Photodermatol Photoimmunol Photomed 23:172-178. (Pubitemid 47354708)
13. Prystowsky JH, PJ Muzio, S Sevran and TL Clemens. (1996). Effect of UVB phototherapy and oral calcitriol (1,25- ihydroxyvitamin D3) on vitamin D photosynthesis in patients with psoriasis. J Am Acad Dermatol 35:690-695. (Pubitemid 26389466)
14. Kim EJ, YK Kim, JE Kim, S Kim, MK Kim, CH Park and JH Chung. (2011). UV modulation of subcutaneous fat metabolism. J Invest Dermatol 131:1720-1726.
15. Kim WS, BS Park, JH Sung, JM Yang, SB Park, SJ Kwak and JS Park. (2007). Wound healing effect of adipose-derived stem cells: a critical role of secretory factors on human dermal fibroblasts. J Dermatol Sci 48:15-24.
16. Kwack MH, SH Shin, SR Kim, SU Im, IS Han, MK Kim, JC Kim and YK Sung. (2009). l-Ascorbic acid 2-phosphate promotes elongation of hair shafts via the secretion of insulin-like growth factor-1 from dermal papilla cells through phosphatidylinositol 3-kinase. Br J Dermatol 160:1157-1162.
17. Venge P. (1979). Kinetic studies of cell migration in a modified Boyden chamber: dependence on cell concentration and effects of the chymotrypsin-like cationic protein of human granulocytes. J Immunol 122:1180-1184. (Pubitemid 9178738)
18. Park SH, YM Jeong, JH Kim, HM Chung, W Suh, SH Sung, SG Park and JH Sung. (2011). Activation of vasculogenic progenitor cells by ent-16alpha,17- dihydroxy-kauran-19-oic acid. Biol Pharm Bull 34:1801-1807.
19. Kim WS, BS Park, HK Kim, JS Park, KJ Kim, JS Choi, SJ Chung, DD Kim and JH Sung. (2008). Evidence supporting antioxidant action of adipose-derived stem cells: protection of human dermal fibroblasts from oxidative stress. J Dermatol Sci 49:133-142.
20. Kwack MH, YK Sung, EJ Chung, SU Im, JS Ahn, MK Kim and JC Kim. (2008). Dihydrotestosterone-inducible dickkopf 1 from balding dermal papilla cells causes apoptosis in follicular keratinocytes. J Invest Dermatol 128:262-269.
21. Muller-Rover S, B Handjiski, C van der Veen, S Eichmuller, K Foitzik, IA McKay, KS Stenn and R Paus. (2001). A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol 117:3-15. (Pubitemid 32652434)
22. Ozeki M and Y Tabata. (2002). Promoted growth of murine hair follicles through controlled release of vascular endothelial growth factor. Biomaterials 23:2367-2373. (Pubitemid 34234838)
23. Yano K, LF Brown and M Detmar. (2001). Control of hair growth and follicle size by VEGF-mediated angiogenesis. J Clin Invest 107:409-417. (Pubitemid 32167987)
24. Ozeki M and Y Tabata. (2002). Promoted growth of murine hair follicles through controlled release of basic fibroblast growth factor. Tissue Eng 8:359-366. (Pubitemid 34747794)
25. Jindo T, R Tsuboi, R Imai, K Takamori, JS Rubin and H Ogawa. (1994). Hepatocyte growth factor/scatter factor stimulates hair growth of mouse vibrissae in organ culture. J Invest Dermatol 103:306-309. (Pubitemid 24329748)
26. Jindo T, R Imai, R Tsuboi, K Takamori and H Ogawa. (1994). The effect of various cytokines on hair growth of mouse vibrissae in organ culture. J Dermatol Sci 7 Suppl 1:S73-S78.
27. Tomita Y, M Akiyama and H Shimizu. (2006). PDGF isoforms induce and maintain anagen phase of murine hair follicles. J Dermatol Sci 43:105-115. (Pubitemid 44094003)
28. Danilenko DM, BD Ring, D Yanagihara, W Benson, B Wiemann, CO Starnes and GF Pierce. (1995). Keratinocyte growth factor is an important endogenous mediator of hair follicle growth, development, and differentiation. Normalization of the nu/nu follicular differentiation defect and amelioration of chemotherapy-induced alopecia. Am J Pathol 147:145-154.
29. Sampat SR, GD O'Connell, JV Fong, E Alegre-Aguaron, GA Ateshian and CT Hung. (2011). Growth factor priming of synovium-derived stem cells for cartilage tissue engineering. Tissue Eng Part A 17:2259-2265.
30. Hwang NS, SG Im, PB Wu, DA Bichara, X Zhao, MA Randolph, R Langer and DG Anderson. (2011). Chondrogenic priming adipose-mesenchymal stem cells for cartilage tissueregeneration. Pharm Res 28:1395-1405.
31. Kim MS, CS Lee, J Hur, HJ Cho, SI Jun, TY Kim, SW Lee, JW Suh, KW Park, et al. (2009). Priming with angiopoietin-1 augments the vasculogenic potential of the peripheral blood stem cells mobilized with granulocyte colony-stimulating factor through a novel Tie2/Ets-1 pathway. Circulation 120:2240-2250.
32. Aly A, K Peterson, A Lerman, L Lerman and M Rodriguez- orcel. (2011). Role of oxidative stress in hypoxia preconditioning of cells transplanted to the myocardium: a molecular imaging study. J Cardiovasc Surg (Torino) 52: 579-585.
33. Stubbs SL, ST Hsiao, HM Peshavariya, SY Lim, GJ Dusting and RJ Dilley. (2012). Hypoxic preconditioning enhances survival of human adipose-derived stem cells and conditions endothelial cells in vitro. Stem Cells Dev 21:1887- 1896.
34. Park BS, WS Kim, JS Choi, HK Kim, JH Won, F Ohkubo and H Fukuoka. (2010). Hair growth stimulated by conditioned medium of adipose-derived stem cells is enhanced by hypoxia:evidence of increased growth factor secretion. Biomed Res 31:27-34.
35. Crop MJ, CC Baan, SS Korevaar, JN Ijzermans, M Pescatori, AP Stubbs, WF van Ijcken, MH Dahlke, E Eggenhofer, W Weimar and MJ Hoogduijn. (2010). Inflammatory conditions affect gene expression and function of human adipose tissue- derived mesenchymal stem cells. Clin Exp Immunol 162: 474-486.
36. Valle-Prieto A and PA Conget. (2010). Human mesenchymal stem cells efficiently manage oxidative stress. Stem Cells Dev 19:1885-1893.
37. Dernbach E, C Urbich, RP Brandes, WK Hofmann, AM Zeiher and S Dimmeler. (2004). Antioxidative stressassociated genes in circulating progenitor cells: evidence for enhanced resistance against oxidative stress. Blood 104: 3591-3597. (Pubitemid 39564432)
38. Le Belle JE, NM Orozco, AA Paucar, JP Saxe, J Mottahedeh, AD Pyle, H Wu and HI Kornblum. (2011). Proliferative neural stem cells have high endogenous ROS levels thatregulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 8:59-71.
39. Ushio-Fukai M and N Urao. (2009). Novel role of NADPH oxidase in angiogenesis and stem/progenitor cell function. Antioxid Redox Signal 11:2517-2533.
40. Lange S, J Heger, G Euler, M Wartenberg, HM Piper and H Sauer. (2009). Platelet-derived growth factor BB stimulatesvasculogenesis of embryonic stem cell-derived endothelial cells by calcium-mediated generation of reactive oxygen species. Cardiovasc Res 81:159-168.
41. Urao N, H Inomata, M Razvi, HW Kim, K Wary, R McKinney, T Fukai and M Ushio-Fukai. (2008). Role of nox2- based NADPH oxidase in bone marrow and progenitor cellfunction involved in neovascularization induced by hindlimb ischemia. Circ Res 103:212-220.
42. Sahara M, M Sata, T Morita, T Nakajima, Y Hirata and R Nagai. (2010). A phosphodiesterase-5 inhibitor vardenafil enhances angiogenesis through a protein kinase G-dependent hypoxia-inducible factor-1/vascular endothelial growth factor pathway. Arterioscler Thromb Vasc Biol 30:1315-1324.
43. Ii M, H Nishimura, A Iwakura, A Wecker, E Eaton, T Asahara and DW Losordo. (2005). Endothelial progenitor cells are rapidly recruited to myocardium and mediate protectiveeffect of ischemic preconditioning via ''imported'' nitric oxide synthase activity. Circulation 111:1114-1120. (Pubitemid 40365471)