Impact of low oxygen on the secretome of human adipose-derived stromal/stem cell primary cultures

Biochimie

Volumn 95, Issue 12, 2013, Pages 2286-2296

  Frazier, Trivia P ^a   Gimble, Jeffrey M ^b   Kheterpal, Indu ^b   Rowan, Brian G ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Extracellular matrix (ECM) remodeling protein secretions and ASCs; Low oxygen culture and adipose derived stromal stem cell (ASC) secretome; Tissue fibrosis and inflammation

Indexed keywords

CD40 LIGAND; COLLAGEN TYPE 1; FIBRONECTIN; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEONECTIN; OXYGEN; PROTEOME; RANTES; SECRETOME; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ADIPOSE DERIVED STEM CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; FEMALE; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; PRIMARY CELL CULTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

2-D; ADIPOSE TISSUE-DERIVED STROMAL/STEM CELLS; ASCS; CD40 L; CD40 LIGAND; COL1Α1; COL1Α2; COLLAGEN TYPE 1Α1; COLLAGEN TYPE Α2; DMEM; DULBECCO'S MODIFIED EAGLE'S MEDIUM; ECM; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX (ECM) REMODELING PROTEIN SECRETIONS AND ASCS; FALSE DISCOVERY RATE; FBS; FDR; FETAL BOVINE SERUM; HIF-1Α; HYPOXIA-INDUCIBLE FACTOR-1Α; IFN-Γ; IL-1Β; IL-4,6,10,13; INTERFERON-GAMMA; INTERLEUKIN-1Β; INTERLEUKINS-4, -6, -10, AND -13; LC-MS/MS; LIQUID CHROMATOGRAPHY AND TANDEM MASS SPECTROMETRY; LOW OXYGEN CULTURE AND ADIPOSE-DERIVED STROMAL/STEM CELL (ASC) SECRETOME; MCP-1; MONOCYTE CHEMOTACTIC PROTEIN-1; PAI-1; PLASMINOGEN ACTIVATOR INHIBITOR-TYPE 1; QRT-PCR; QUANTITATIVE REVERSE-TRANSCRIPTASE POLYMERASE CHAIN REACTION; RECEIVER OPERATING CHARACTERISTIC CURVE; ROC CURVE; SECRETED PROTEIN ACIDIC, CYSTEINE-RICH; SERINE PROTEASE INHIBITORS; SERPINS; SPARC/OSTEONECTIN; STROMAL VASCULAR FRACTION; SVF; TGF-Β1-INDUCED PROTEIN; TISSUE FIBROSIS AND INFLAMMATION; TNF-Α; TUMOR NECROSIS FACTOR-Α; TWO-DIMENSIONAL; WAT; WHITE ADIPOSE TISSUE; ΒIG-H3;

ADIPOCYTES; ADIPOSE TISSUE; ADULT; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; CYTOKINES; EXTRACELLULAR MATRIX PROTEINS; FEMALE; FIBROSIS; HUMANS; INTERLEUKIN-6; MIDDLE AGED; OXYGEN; PROTEOME; STEM CELLS; TANDEM MASS SPECTROMETRY;

EID: 84887820593     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2013.07.011     Document Type: Article

References (76)

1. C. Alexakis, J.P. Caruelle, A. Sezeur, J. Cosnes, J.P. Gendre, H. Mosnier, L. Beaugerie, D. Gallot, M. Malafosse, D. Barritault, and P. Kern Reversal of abnormal collagen production in Crohn's disease intestinal biopsies treated with regenerating agents Gut 53 2004 85 90
2. G.C. Carvalho, C.A. Regis, J.R. Kalil, L.A. Cerqueira, D.S. Barbosa, M.P. Motta, N.M. da Silva, M.A. Pires Soares, C.C. Zollinger, and P.L. Bittencourt Causes of renal failure in patients with decompensated cirrhosis and its impact in hospital mortality Ann. Hepatol. 11 2012 90 95
3. J. Hua-liang, and D. Jing-cheng Pathogenesis of idiopathic fibrosis: from initial apoptosis of epithelial cells to lung remodeling? China Med. 24 2011 4330 4338
4. G.C. Ribeiro, M. Lopes, F. Antoniali, A. Nunes, C.E. Costa, and J.L. Fernandes Importance of the area of fibrosis at midterm evolution of patients submitted to ventricular reconstruction Arq. Bras. Cardiol. 93 2009 564 566
5. L. Rifai, N. Hammoudi, P. Fouret, and C. Acar Massive calcification of the tricuspid valve papillary muscles in right ventricular endomyocardial fibrosis Interact. Cardiovasc. Thorac. Surg. 12 2011 505 506
6. P.L. Sinn, R.M. Anthony, and P.B. McCray Jr. Genetic therapies for cystic fibrosis lung disease Hum. Mol. Genet. 20 2011 R79 R86
7. M.M. Abdelaziz, Y.S. Samman, S.O. Wali, and M.M. Hamad Treatment of idiopathic pulmonary fibrosis: is there anything new? Respirology 10 2005 284 289
8. S. Tome, and M.R. Lucey Current management of alcoholic liver disease Aliment. Pharmacol. Ther. 19 2004 707 714
9. M. Gharaee-Kermani, and S.H. Phan Role of cytokines and cytokine therapy in wound healing and fibrotic diseases Curr. Pharm. Des. 7 2001 1083 1103
10. M. Gharaee-Kermani, B. Hu, V.J. Thannickal, S.H. Phan, and M.R. Gyetko Current and emerging drugs for idiopathic pulmonary fibrosis Expert Opin. Emerg. Drugs 12 2007 627 646
11. S. Mutalik Treatment of keloids and hypertrophic scars Indian J. Dermatol. Venereol. Leprol. 71 2005 3 8
12. C. Bouffi, F. Djouad, M. Mathieu, D. Noel, and C. Jorgensen Multipotent mesenchymal stromal cells and rheumatoid arthritis: risk or benefit? Rheumatology (Oxford) 48 2009 1185 1189
13. F. Djouad, C. Bouffi, S. Ghannam, D. Noel, and C. Jorgensen Mesenchymal stem cells: innovative therapeutic tools for rheumatic diseases Nat. Rev. Rheumatol. 5 2009 392 399
14. M. Gharaee-Kermani, M.R. Gyetko, B. Hu, and S.H. Phan New insights into the pathogenesis and treatment of idiopathic pulmonary fibrosis: a potential role for stem cells in the lung parenchyma and implications for therapy Pharm. Res. 24 2007 819 841
15. S.S. Iyer, C. Co, and M. Rojas Mesenchymal stem cells and inflammatory lung diseases Panminerva Med. 51 2009 5 16
16. C. Roufosse, G. Bou-Gharios, E. Prodromidi, C. Alexakis, R. Jeffery, S. Khan, W.R. Otto, J. Alter, R. Poulsom, and H.T. Cook Bone marrow-derived cells do not contribute significantly to collagen I synthesis in a murine model of renal fibrosis J. Am. Soc. Nephrol. 17 2006 775 782
17. D.J. Weiss, I. Bertoncello, Z. Borok, C. Kim, A. Panoskaltsis-Mortari, S. Reynolds, M. Rojas, B. Stripp, D. Warburton, and D.J. Prockop Stem cells and cell therapies in lung biology and lung diseases Proc. Am. Thorac. Soc. 8 2011 223 272
18. L. Cai, B.H. Johnstone, T.G. Cook, J. Tan, M.C. Fishbein, P.-S. Chen, and K.L. March IFATS collection: human adipose tissue-derived stem cells induce angiogenesis and nerve sprouting following myocardial infarction, in conjunction with potent preservation of cardiac function Stem Cells 1 2009 230 237
19. H. Tapp, R. Deepe, J.A. Ingram, M. Kuremsky, E.N. Hanley Jr., and H.E. Gruber Adipose-derived mesenchymal stem cells from the sand rat: transforming growth factor beta and 3D co-culture with human disc cells stimulate proteoglycan and collagen type I rich extracellular matrix Arthritis Res. Ther. 10 2008 R89
20. H. Tapp, E.N. Hanley Jr., J.C. Patt, and H.E. Gruber Adipose-derived stem cells: characterization and current application in orthopaedic tissue repair Exp. Biol. Med. (Maywood) 234 2009 1 9
21. P. Semedo, M. Correa-Costa, C.M. Antonio, M.D. Maria Avancini Costa, R.M. Antonia dos, M.H. Shimizu, A.C. Seguro, A. Pacheco-Silva, and N.O. Saraiva Camara Mesenchymal stem cells attenuate renal fibrosis through immune modulation and remodeling properties in a rat remnant kidney model Stem Cells 27 2009 3063 3073
22. C. Donizetti-Oliveira, P. Senedo, M. Burgos-Silva, M.A. Cenedeze, D.M.A.C. Malheiros, M.A. Reis, A. Pacheco-Silva, and M.O.S. Camara Adipose tissue-derived stem cell treatment prevents renal disease progression Cell Transplant. 8 2011 1727 1741
23. M. Nambu, M. Ishihara, S. Nakamura, H. Mizuno, S. Yanagibayashi, Y. Kanatani, H. Hattori, B. Takase, T. Ishizuka, S. Kishimoto, Y. Amano, N. Yamamoto, R. Azuma, and T. Kiyosawa Enhanced healing of mitomycin C-treated wounds in rats using inbred adipose tissue-derived stromal cells within an atelocollagen matrix Wound Repair Regen. 15 2007 505 510
24. Y. Miyahara, N. Nagaya, M. Kataoka, B. Yanagawa, K. Tanaka, H. Hao, K. Ishino, H. Ishida, T. Shimizu, K. Kangawa, S. Sano, T. Okano, S. Kitamura, and H. Mori Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction Nat. Med. 4 2006 459 465
25. K. Schenke-Layland, B.M. Strem, M.C. Jordan, M.T. Deemedio, M.H. Hedrick, K.P. Roos, J.K. Fraser, and W.R. Maclellan Adipose tissue-derived cells improve cardiac function following myocardial infarction J. Surg. Res. 2 2009 217 223
26. S.K. Kang, D.H. Lee, Y.C. Bae, H.K. Kim, S.Y. Baik, and J.S. Jung Exp. Neurol. 4 2003 691 708
27. J. Rehman, D. Traktuev, J. Li, S. Merfeld-Clauss, C.J. Temm-Grove, J.E. Bovenkerk, C.L. Pell, B.H. Johnstone, R.V. Considine, and K.L. March Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells Circulation 109 2004 1292 1298
28. J.M. Gimble, A.J. Katz, and B.A. Bunnell Adipose-derived stem cells for regenerative medicine Circ. Res. 100 2007 1249 1260
29. H. Skalnikova, J. Motlik, S.J. Gadher, and H. Kovarova Mapping of the secretome of primary isolates of mammalian cells, stem cells and derived cell lines Proteomics 11 2011 691 708
30. P. Scherp, G. Ku, L. Colemanand, and I. Kheterpal Gel-based and gel-free proteomic technologies Methods Mol. Biol. 702 2011 163 190
31. P. Scherp, N. Putluri, G.J. LeBlanc, Z.Q. Wang, X.H. Zhang, Y. Yu, D. Ribnicky, W.T. Cefalu, and I. Kheterpal Proteomic analysis reveals cellular pathways regulating carbohydrate metabolism that are modulated in primary human skeletal muscle culture due to treatment with bioactives from Artemisia dracunculus L. J. Proteomics 75 2012 3199 3210
32. R.H. Pichler, C. Hugo, S.J. Shankland, M.J. Reed, J.A. Bassuk, T.F. Andoh, D.M. Lombardi, S.M. Schwartz, W.M. Bennett, C.E. Alpers, E.H. Sage, R.J. Johnson, and W.G. Couser SPARC is expressed in renal interstitial fibrosis and in renal vascular injury Kidney Int. 50 1996 1978 1989
33. R.H. Pichler, J.A. Bassuk, C. Hugo, M.J. Reed, E. Eng, K.L. Gordon, J. Pippin, C.E. Alpers, W.G. Couser, E.H. Sage, and R.J. Johnson SPARC is expressed by mesangial cells in experimental mesangial proliferative nephritis and inhibits platelet-derived-growth-factor-medicated mesangial cell proliferation in vitro Am. J Pathol. 148 1996 1153 1167
34. M.J. Socha, M. Manhiani, N. Said, J.D. Imig, and K. Motamed Secreted protein acidic and rich in cysteine deficiency ameliorates renal inflammation and fibrosis in angiotensin hypertension Am. J Pathol. 171 2007 1104 1112
35. J. Trombetta-Esilva, and A.D. Bradshaw The function of SPARC as a mediator of fibrosis Open. Rheumatol. J. 6 2012 146 155
36. N. Hosogai, A. Fukuhara, K. Oshima, Y. Miyata, S. Tanaka, K. Segawa, S. Furukawa, Y. Tochino, R. Komuro, M. Matsuda, and I. Shimomura Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation Diabetes 56 2007 901 911
37. K.M. Moon, Y.H. Park, J.S. Lee, Y.B. Chae, M.M. Kim, D.S. Kim, B.W. Kim, S.W. Nam, and J.H. Lee The effect of secretory factors of adipose-derived stem cells on human keratinocytes Int. J. Mol. Sci. 13 2012 1239 1257
38. K. Hida, J. Wada, J. Eguchi, H. Zhang, M. Baba, A. Seida, I. Hashimoto, T. Okada, A. Yasuhara, A. Nakatsuka, K. Shikata, S. Hourai, J. Futami, E. Watanabe, Y. Matsuki, R. Hiramatsu, S. Akagi, H. Makino, and Y.S. Kanwar Visceral adipose tissue-derived serine protease inhibitor: a unique insulin-sensitizing adipocytokine in obesity Proc. Natl. Acad. Sci. U. S. A. 102 2005 10610 10615
39. F. Samad, K. Yamamoto, and D.J. Loskutoff Distribution and regulation of plasminogen activator inhibitor-1 in murine adipose tissue in vivo. Induction by tumor necrosis factor-alpha and lipopolysaccharide J. Clin. Invest. 97 1996 37 46
40. S. Zvonic, M. Lefevre, G. Kilroy, Z.E. Floyd, J.P. DeLany, I. Kheterpal, A. Gravois, R. Dow, A. White, X. Wu, and J.M. Gimble Secretome of primary cultures of human adipose-derived stem cells: modulation of serpins by adipogenesis Mol. Cell. Proteomics 6 2007 18 28
41. J.E. Celis, J.M. Moreira, T. Cabezon, P. Gromov, E. Friis, F. Rank, and I. Gromova Identification of extracellular and intracellular signaling components of the mammary adipose tissue and its interstitial fluid in high risk breast cancer patients: toward dissecting the molecular circuitry of epithelial-adipocyte stromal cell interactions Mol. Cell. Proteomics 4 2005 492 522
42. I. Kratchmarova, D.E. Kalume, B. Blagoev, P.E. Scherer, A.V. Podtelejnikov, H. Molina, P.E. Bickel, J.S. Andersen, M.M. Fernandez, J. Bunkenborg, P. Roepstorff, K. Kristiansen, H.F. Lodish, M. Mann, and A. Pandey A proteomic approach for identification of secreted proteins during the differentiation of 3T3-L1 preadipocytes to adipocytes Mol. Cell. Proteomics 1 2002 213 222
43. H. Nielsen, J. Engelbrecht, S. Brunak, and H.G. von Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites Protein Eng. 10 1997 1 6
44. A. Abderrahim-Ferkoune, O. Bezy, C. Chiellini, M. Maffei, P. Grimaldi, F. Bonino, N. Moustaid-Moussa, F. Pasqualini, A. Mantovani, G. Ailhaud, and E.Z. Amri Characterization of the long pentraxin PTX3 as a TNFalpha-induced secreted protein of adipose cells J. Lipid Res. 44 2003 994 1000
45. M.C. Sanchez, G.A. Chiabrando, and M.A. Vides Pregnancy zone protein-tissue-type plasminogen activator complexes bind to low-density lipoprotein receptor-related protein (LRP) Arch. Biochem. Biophys. 389 2001 218 222
46. X. Chen, S.W. Cushman, L.K. Pannell, and S. Hess Quantitative proteomic analysis of the secretory proteins from rat adipose cells using a 2D liquid chromatography-MS/MS approach J. Proteome Res. 4 2005 570 577
47. C. Buttner, A. Skupin, T. Reimann, E.P. Rieber, G. Unteregger, P. Geyer, and K.H. Frank Local production of interleukin-4 during radiation-induced pneumonitis and pulmonary fibrosis in rats: macrophages as a prominent source of interleukin-4 Am. J Respir. Cell Mol.Biol. 17 1997 315 325
48. F. Huaux, M. Arras, A. Vink, J.C. Renauld, and D. Lison Soluble tumor necrosis factor (TNF) receptors p55 and p75 and interleukin-10 downregulate TNF-alpha activity during the lung response to silica particles in NMRI mice Am. J. Respir. Cell Mol. Biol. 21 1999 137 145
49. P.J. Sime, and K.M.A. O'Reilly Fibrosis of the lung and other tissues: new concepts in pathogenesis and treatment Clin. Immunol. 3 2001 308 319
50. E.P. Brennan, M.J. Morine, D.W. Walsh, S.A. Roxburgh, M.T. Lindenmeyer, D.P. Brazil, P.O. Gaora, H.M. Roche, D.M. Sadlier, C.D. Cohen, C. Godson, and F. Martin Next-generation sequencing identifies TGF-β1-associated gene expression profiles in renal epithelial cells reiterated in human diabetic nephropathy Biochim. Biophys. Acta 1822 2012 589 599
51. K.E. Nakken, S. Nygard, T. Haaland, K.E. Berge, K. Arnkvaern, A. Odegaard, K.J. Labori, and M.G. Raeder Multiple inflammatory-, tissue remodelling- and fibrosis genes are differentially transcribed in the livers of Abcb4 (-/-) mice harbouring chronic cholangitis Scand. J. Gastroenterol. 42 2007 1245 1255
52. R. Bataller, and D.A. Brenner Liver fibrosis J. Clin. Invest. 115 2005 209 218
53. R.F. Diegelmann, and M.C. Evans Wound healing: an overview of acute, fibrotic and delayed healing Front. Biosci. 9 2004 283 289
54. T.N. Wight, and S. Potter-Perigo The extracellular matrix: an active or passive player in fibrosis? Am. J. Physiol. Gastrointest. Liver Physiol. 6 2011 G950 G955
55. D. Anglicheau, T. Muthukumar, A. Hummel, R. Ding, V.K. Sharma, D. Dadhania, S.V. Seshan, J.E. Schwartz, and M. Suthanthiran Discovery and validation of a molecular signature for the noninvasive diagnosis of human renal allograft fibrosis Clin. Translational Res. 11 2012 1136 1146
56. C. Henegar, J. Tordjman, V. Achard, D. Lacasa, I. Cremer, M. Guerre-Millo, C. Poitou, A. Basdevant, V. Stich, N. Viguerie, D. Langin, P. Bedossa, J.D. Zucker, and K. Clement Adipose tissue transcriptomic signature highlights the pathological relevance of extracellular matrix in human obesity Genome Biol. 9 2008 R14
57. X. Hu, S.P. Yu, J.L. Fraser, Z. Lu, M.E. Ogle, J.A. Wang, and L. Wei Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis J. Thorac. Cardiovasc. Surg. 135 2008 799 808
58. E.Y. Lee, Y. Xia, W.S. Kim, M.H. Kim, T.H. Kim, K.J. Kim, B.S. Park, and J.H. Sung 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 2009 540 547
59. J.A. Wang, A. He, X. Hu, Y. Jiang, Y. Sun, J. Jiang, C. Gui, Y. Wang, and H. Chen Anoxic preconditioning: a way to enhance the cardioprotection of mesenchymal stem cells Int. J. Cardiol. 133 2009 410 412
60. L. Leroux, B. Descamps, N.F. Tojais, B. Seguy, P. Oses, C. Moreau, D. Daret, Z. Ivanovic, J.M. Boiron, J.M. Lamaziere, P. Dufourcq, T. Couffinhal, and C. Duplaa Hypoxia preconditioned mesenchymal stem cells improve vascular and skeletal muscle fiber regeneration after ischemia through a Wnt4-dependent pathway Mol. Ther. 18 2010 1545 1552
61. I. Rosova, M. Dao, B. Capoccia, D. Link, and J.A. Nolta Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells Stem Cells 26 2008 2173 2182
62. A. Divoux, S. Moutel, C. Poitou, D. Lacasa, N. Veyrie, A. Aissat, M. Arock, M. Guerre-Millo, and K. Clement Mast cells in human adipose tissue: link with morbid obesity, inflammatory status, and diabetes J. Clin. Endocrinol. Metab. 9 2012 E1677 E1685
63. M. Maumus, C. Sengenes, P. Decaunes, A. Zakaroff-Girard, V. Bourlier, M. Lafontan, J. Galitzky, and A. Bouloumie Evidence of in situ proliferation of adult adipose tissue-derived progenitor cells: influence of fat mass microenvironment and growth J. Clin. Endocrinol. Metab. 93 2008 4098 4106
64. K. McIntosh, S. Zvonic, S. Garrett, J.B. Mitchell, Z.E. Floyd, L. Hammill, A. Kloster, H.Y. Di, J.P. Ting, R.W. Storms, B. Goh, G. Kilroy, X. Wu, and J.M. Gimble The immunogenicity of human adipose-derived cells: temporal changes in vitro Stem Cells 24 2006 1246 1253
65. J.B. Mitchell, K. McIntosh, S. Zvonic, S. Garrett, Z.E. Floyd, A. Kloster, H.Y. Di, R.W. Storms, B. Goh, G. Kilroy, X. Wu, and J.M. Gimble Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers Stem Cells 24 2006 376 385
66. P.H. Oliveira, J.S. Boura, M.M. Abecasis, J.M. Gimble, C.L. da Silva, and J.M. Cabral Impact of hypoxia and long-term cultivation on the genomic stability and mitochondrial performance of ex vivo expanded human stem/stromal cells Stem Cell Res. 9 2012 225 236
67. X.-Y. Jiang, D.-B. Lu, Y.-Z. Jiang, L.-N. Zhou, L.-Q. Cheng, and B. Chen PGC-1α prevents apoptosis in adipose-derived stem cells by reducing reactive oxygen species production in a diabetic microenvironment Diabetes Res. Clin. Pract. 100 2013 368 375
68. W. Zhu, J. Chen, X. Cong, S. Hu, and X. Chen Hypoxia and serum deprivation-induced apoptosis in mesenchymal stem cells Stem Cells 2 2006 416 425
69. R.M. Gallucci, D.K. Sloan, J.M. Heck, A.R. Murray, and S.J. O'Dell Interleukin 6 indirectly induces keratinocyte migration J. Invest. Dermatol. 122 2004 764 772
70. W.S. Kim, B.S. Park, J.H. Sung, J.M. Yang, S.B. Park, S.J. Kwak, and J.S. Park Wound healing effect of adipose-derived stem cells: a critical role of secretory factors on human dermal fibroblasts J. Dermatol. Sci. 48 2007 15 24
71. W.S. Kim, B.S. Park, and J.H. Sung The wound-healing and antioxidant effects of adipose-derived stem cells Expert Opin. Biol. Ther. 9 2009 879 887
72. L.R. Luckett-Chastain, and R.M. Gallucci Interleukin (IL)-6 modulates transforming growth factor-beta expression in skin and dermal fibroblasts from IL-6-deficient mice Br. J. Dermatol. 161 2009 237 248
73. + cells and increases IL-10 secretion J. Biomed. Biotechnol. 2012 2012 295167
74. T. Nakashima, M. Jinnin, K. Yamane, N. Honda, I. Kajihara, T. Makino, S. Masuguchi, S. Fukushima, Y. Okamoto, M. Hasegawa, M. Fujimoto, and H. Ihn Impaired IL-17 signaling pathway contributes to the increased collagen expression in scleroderma fibroblasts J. Immunol. 188 2012 3573 3583
75. T.R. Mosmann, H. Cherwinski, M.W. Bond, M.A. Giedlin, and R.L. Coffman Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins J. Immunol. 136 1986 2348 2357
76. K.M. Moon, Y.H. Park, S.J. Lee, Y.B. Chae, M.-M. Kim, D.-S. Kim, B.-W. Kim, S.W. Nam, and J.-H. Lee The effect of secretory factors of adipose-serived stem cells on human keratinocytes Int J Mol. Sci. 13 2012 1239 1257