Direct comparison of the potency of human mesenchymal stem cells derived from amnion tissue, bone marrow and adipose tissue at inducing dermal fibroblast responses to cutaneous wounds

Liu,Xiaoyu; Wang,Zhe; Wang,Rui; Zhao,Feng; Shi,Ping; Jiang,Yide; Pang,Xining

doi:10.3892/ijmm.2012.1199

February 2013 Volume 31 Issue 2

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February 2013 Volume 31 Issue 2

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Article

Direct comparison of the potency of human mesenchymal stem cells derived from amnion tissue, bone marrow and adipose tissue at inducing dermal fibroblast responses to cutaneous wounds

Authors:
- Xiaoyu Liu
- Zhe Wang
- Rui Wang
- Feng Zhao
- Ping Shi
- Yide Jiang
- Xining Pang
View Affiliations / Copyright

Affiliations: Key Laboratory of Cell Biology, Ministry of Public Health of China, Department of Stem Cells and Regenerative Medicine, The First Affiliated Hospital, China Medical University, Shenyang, Liaoning 110001, P.R. China, Department of General Practice, The First Affiliated Hospital, China Medical University, Shenyang, Liaoning 110001, P.R. China
Pages: 407-415
|
Published online on: November 30, 2012

https://doi.org/10.3892/ijmm.2012.1199
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Abstract

Although transplantation of human mesenchymal stem cells (MSCs) derived from amnion (hAMSCs), bone marrow (hBMSCs) and adipose tissues (hADSCs) has been shown to aid in the repair of cutaneous wounds in mouse models, little information is available regarding the relative efficacy of MSCs from different sources. In this study, we compared their therapeutic potentials by transplanting equal numbers of hAMSCs, hBMSCs or hADSCs in a mouse model of cutaneous wounds. The results suggested that an hADSC injection has the most pronounced effect on wound closure. Histological evaluation showed enhanced re-epithelialization in the hADSC group compared with the hBMSC and hAMSC groups. Although there was a slight improvement in wound healing in the hAMSC and hBMSC groups, the differences between the groups were statistically insignificant. In a trans-well coculture model, wound healing migration and transwell migration assays showed that hADSCs were superior to hAMSCs and hBMSCs at promoting human dermal fibroblast (hDF) migration. However, there was no significant difference in fibroblast proliferation between the hAMSC, hBMSC and hADSC groups, as measured by WST assay. Our results also indicated that hDFs cocultured with hADSCs for 48 h significantly upregulated their mRNA expression of the cytokine vascular endothelial growth factor, basic fibroblast growth factor, keratinocyte growth factor and transforming growth factor-β and increased the mRNA and protein levels of type I collagen. Collectively, these data suggest that hADSCs are a potential source of MSCs for therapeutic healing in cutaneous wounds in terms of efficacy, accessibility and availability.

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1.	Chen M, Przyborowski M and Berthiaume F: Stem cells for skin tissue engineering and wound healing. Crit Rev Biomed Eng. 37:399–421. 2009. View Article : Google Scholar : PubMed/NCBI
2.	Walter MN, Wright KT, Fuller HR, MacNeil S and Johnson WE: Mesenchymal stem cell-conditioned medium accelerates skin wound healing: an in vitro study of fibroblast and keratinocyte scratch assays. Exp Cell Res. 316:1271–1281. 2010. View Article : Google Scholar : PubMed/NCBI
3.	Han SK, Yoon TH, Lee DG, Lee MA and Kim WK: Potential of human bone marrow stromal cells to accelerate wound healing in vitro. Ann Plast Surg. 55:414–419. 2005. View Article : Google Scholar : PubMed/NCBI
4.	Kim Y, Kim H, Cho H, Bae Y, Suh K and Jung J: Direct comparison of human mesenchymal stem cells derived from adipose tissues and bone marrow in mediating neovascularization in response to vascular ischemia. Cell Physiol Biochem. 20:867–876. 2007. View Article : Google Scholar : PubMed/NCBI
5.	Prockop DJ: Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 276:71–74. 1997. View Article : Google Scholar : PubMed/NCBI
6.	Pittenger MF, Mackay AM, Beck SC, et al: Multilineage potential of adult human mesenchymal stem cells. Science. 284:143–147. 1999. View Article : Google Scholar : PubMed/NCBI
7.	Zuk PA, Zhu M, Mizuno H, et al: Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 7:211–228. 2001. View Article : Google Scholar : PubMed/NCBI
8.	Safford KM, Hicok KC, Safford SD, et al: Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem Biophys Res Commun. 294:371–379. 2002. View Article : Google Scholar : PubMed/NCBI
9.	Reyes M, Dudek A, Jahagirdar B, Koodie L, Marker PH and Verfaillie CM: Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest. 109:337–346. 2002. View Article : Google Scholar : PubMed/NCBI
10.	Smith AN, Willis E, Chan VT, Muffley LA, Isik FF, Gibran NS and Hocking AM: Mesenchymal stem cells induce dermal fibroblast responses to injury. Exp Cell Res. 316:48–54. 2010. View Article : Google Scholar : PubMed/NCBI
11.	Xing L, Franz MG, Marcelo CL, Smith CA, Marshall VS and Robson MC: Amnion-derived multipotent progenitor cells increase gain of incisional breaking strength and decrease incidence and severity of acute wound failure. J Burns Wounds. 7:e52007.PubMed/NCBI
12.	Kim SS, Song CK, Shon SK, Lee KY, Kim CH, Lee MJ and Wang L: Effects of human amniotic membrane grafts combined with marrow mesenchymal stem cells on healing of full-thickness skin defects in rabbits. Cell Tissue Res. 336:59–66. 2009. View Article : Google Scholar : PubMed/NCBI
13.	Jung KH, Song SU, Yi T, et al: Human bone marrow-derived clonal mesenchymal stem cells inhibit inflammation and reduce acute pancreatitis in rats. Gastroenterology. 140:998–1008. 2011. View Article : Google Scholar : PubMed/NCBI
14.	Saito T, Kuang JQ, Bittira B, Al-Khaldi A and Chiu RC: Xenotransplant cardiac chimera: immune tolerance of adult stem cells. Ann Thorac Surg. 74:19–24. 2002. View Article : Google Scholar : PubMed/NCBI
15.	Kim WS, Park BS, Sung JH, et al: Wound healing effect of adipose-derived stem cells: a critical role of secretory factors on human dermal fibroblasts. J Dermatol Sci. 48:15–24. 2007. View Article : Google Scholar : PubMed/NCBI
16.	Falanga V, Iwamoto S, Chartier M, et al: Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. Tissue Eng. 13:1299–1312. 2007. View Article : Google Scholar : PubMed/NCBI
17.	Javazon EH, Keswani SG, Badillo AT, et al: Enhanced epithelial gap closure and increased angiogenesis in wounds of diabetic mice treated with adult murine bone marrow stromal progenitor cells. Wound Repair Regen. 15:350–359. 2007. View Article : Google Scholar : PubMed/NCBI
18.	Lin CD, Allori AC, Macklin JE, et al: Topical lineage-negative progenitor-cell therapy for diabetic wounds. Plast Reconstr Surg. 122:1341–1351. 2008. View Article : Google Scholar : PubMed/NCBI
19.	Wu Y, Chen L, Scott PG and Tredget EE: Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells. 25:2648–2659. 2007. View Article : Google Scholar : PubMed/NCBI
20.	Wu Y, Wang JF, Scott PG and Tredget EE: Bone marrow-derived stem cells in wound healing: a review. Wound Repair Regen. 15(Suppl 1): S18–S26. 2007. View Article : Google Scholar : PubMed/NCBI
21.	Sasaki M, Abe R, Fujita Y, Ando S, Inokuma D and Shimizu H: Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell type. J Immunol. 180:2581–2587. 2008. View Article : Google Scholar : PubMed/NCBI
22.	Yoo JH, Park C, Jung DI, et al: In vivo cell tracking of canine allogenic mesenchymal stem cells administration via renal arterial catheterization and physiopathological effects on the kidney in two healthy dogs. J Vet Med Sci. 73:269–274. 2011. View Article : Google Scholar
23.	Balakumaran A, Pawelczyk E, Ren J, et al: Superparamagnetic iron oxide nanoparticles labeling of bone marrow stromal (mesenchymal) cells does not affect their ‘stemness’. PLoS One. 5:e114622010.
24.	Chen L, Tredget EE, Wu PY and Wu Y: Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One. 3:e18862008. View Article : Google Scholar : PubMed/NCBI
25.	Yu M, Cai L, Liang M, et al: Alteration of NRSF expression exacerbating 1-methyl-4-phenyl-pyridinium ion-induced cell death of SH-SY5Y cells. Neurosci Res. 65:236–244. 2009. View Article : Google Scholar : PubMed/NCBI
26.	Li H, Wang L, Ye L, et al: Influence of Pseudomonas aeruginosa quorum sensing signal molecule N-(3-oxododecanoyl) homoserine lactone on mast cells. Med Microbiol Immunol. 198:113–121. 2009.
27.	Cheng Y, Hu R, Jin H, et al: Effect of 14-3-3 tau protein on differentiation in BeWo choriocarcinoma cells. Placenta. 31:60–66. 2010. View Article : Google Scholar : PubMed/NCBI
28.	Liu S, Yang P, Kang H, et al: NDRG2 induced by oxidized LDL in macrophages antagonizes growth factor productions via selectively inhibiting ERK activation. Biochim Biophys Acta. 1801:106–113. 2010. View Article : Google Scholar : PubMed/NCBI
29.	Wagner W, Wein F, Seckinger A, et al: Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol. 33:1402–1416. 2005. View Article : Google Scholar : PubMed/NCBI
30.	Hartlapp I, Abe R, Saeed RW, et al: Fibrocytes induce an angiogenic phenotype in cultured endothelial cells and promote angiogenesis in vivo. FASEB J. 15:2215–2224. 2001. View Article : Google Scholar : PubMed/NCBI
31.	Martin P: Wound healing-aiming for perfect skin regeneration. Science. 276:75–81. 1997. View Article : Google Scholar : PubMed/NCBI
32.	Singer AJ and Clark RA: Cutaneous wound healing. N Engl J Med. 341:738–746. 1999. View Article : Google Scholar : PubMed/NCBI
33.	Shojaku H, Takakura H, Okabe M, Fujisaka M, Watanabe Y and Nikaido T: Effect of hyperdry amniotic membrane patches attached over the bony surface of mastoid cavities in canal wall down tympanoplasty. Laryngoscope. 121:1953–1957. 2011.PubMed/NCBI
34.	Gruss JS and Jirsch DW: Human amniotic membrane: a versatile wound dressing. Can Med Assoc J. 118:1237–1246. 1978.PubMed/NCBI
35.	Krishnamurithy G, Shilpa PN, Ahmad RE, Sulaiman S, Ng CL and Kamarul T: Human amniotic membrane as a chondrocyte carrier vehicle/substrate: in vitro study. J Biomed Mater Res A. 99:500–506. 2011. View Article : Google Scholar : PubMed/NCBI
36.	McGhee CN and Patel DV: Mooren’s ulcer and amniotic membrane transplant: a simple surgical solution? Clin Experiment Ophthalmol. 39:383–385. 2011.
37.	Pessolato AG, Martins Ddos S, Ambrósio CE, Mançanares CA and de Carvalho AF: Propolis and amnion reepithelialise second-degree burns in rats. Burns. 37:1192–1201. 2011. View Article : Google Scholar : PubMed/NCBI
38.	Toda A, Okabe M, Yoshida T and Nikaido T: The potential of amniotic membrane/amnion-derived cells for regeneration of various tissues. J Pharmacol Sci. 105:215–228. 2007. View Article : Google Scholar : PubMed/NCBI
39.	Chesney J, Metz C, Stavitsky AB, Bacher M and Bucala R: Regulated production of type I collagen and inflammatory cytokines by peripheral blood fibrocytes. J Immunol. 160:419–425. 1998.PubMed/NCBI
40.	Belgore F, Lip GY and Blann AD: Basic fibroblast growth factor induces the secretion of vascular endothelial growth factor by human aortic smooth muscle cells but not by endothelial cells. Eur J Clin Invest. 33:833–839. 2003. View Article : Google Scholar
41.	Zhang F, Oswald T, Lin S, et al: Vascular endothelial growth factor (VEGF) expression and the effect of exogenous VEGF on survival of a random flap in the rat. Br J Plast Surg. 56:653–659. 2003. View Article : Google Scholar : PubMed/NCBI
42.	Yang R, Thomas GR, Bunting S, et al: Effects of vascular endothelial growth factor on hemodynamics and cardiac performance. J Cardiovasc Pharmacol. 27:838–844. 1996. View Article : Google Scholar : PubMed/NCBI
43.	Barrientos S, Stojadinovic O, Golinko MS, Brem H and Tomic-Canic M: Growth factors and cytokines in wound healing. Wound Repair Regen. 16:585–601. 2008. View Article : Google Scholar : PubMed/NCBI
44.	Postlethwaite AE, Keski-Oja J, Moses HL and Kang AH: Stimulation of the chemotactic migration of human fibroblasts by transforming growth factor beta. J Exp Med. 165:251–256. 1987. View Article : Google Scholar : PubMed/NCBI
45.	Li Y, Fan J, Chen M, Li W and Woodley DT: Transforming growth factor-alpha: a major human serum factor that promotes human keratinocyte migration. J Invest Dermatol. 126:2096–2105. 2006. View Article : Google Scholar : PubMed/NCBI
46.	Arnold F and West DC: Angiogenesis in wound healing. Pharmacol Ther. 52:407–422. 1991. View Article : Google Scholar
47.	Fam NP, Verma S, Kutryk M and Stewart DJ: Clinician guide to angiogenesis. Circulation. 108:2613–2618. 2003. View Article : Google Scholar : PubMed/NCBI
48.	Hansen SL, Young DM and Boudreau NJ: HoxD3 expression and collagen synthesis in diabetic fibroblasts. Wound Repair Regen. 11:474–480. 2003. View Article : Google Scholar : PubMed/NCBI

Journals

International Journal of Molecular Medicine

International Journal of Oncology

Molecular Medicine Reports

Oncology Reports

Experimental and Therapeutic Medicine

Oncology Letters

Biomedical Reports

Molecular and Clinical Oncology

World Academy of Sciences Journal

International Journal of Functional Nutrition

International Journal of Epigenetics

Medicine International

Direct comparison of the potency of human mesenchymal stem cells derived from amnion tissue, bone marrow and adipose tissue at inducing dermal fibroblast responses to cutaneous wounds

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