Human urine-derived stem cells in combination with polycaprolactone/gelatin nanofibrous membranes enhance wound healing by promoting angiogenesis

Journal of Translational Medicine

Volumn 12, Issue 1, 2014, Pages

  Fu, Yinxin ^a,b   Guan, Junjie ^a   Guo, Shangchun ^a   Guo, Fei ^c   Niu, Xin ^a   Liu, Qiang ^c   Zhang, Changqing ^a   Nie, Huarong ^c,d   Wang, Yang ^a  

^a SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c Jiangxi Origin Bio TECH Co LTD   (China)

^d Jiangxi Chuanqi pharmaceutical Co LTD   (China)

Author keywords

Angiogenesis; Endothelial cells; Human urine derived stem cells (USCs); Polycaprolactone gelatin (PCL GT)

Indexed keywords

BIOMATERIAL; COLLAGEN; GELATIN; POLYCAPROLACTONE; TRANSFORMING GROWTH FACTOR BETA1; VASCULOTROPIN; ARTIFICIAL MEMBRANE; CONDITIONED MEDIUM; NANOFIBER; POLYESTER;

ADIPOCYTE; ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCOMPATIBILITY; CARTILAGE CELL; CELL ADHESION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; COLLAGEN SYNTHESIS; COMPOSITE MATERIAL; CONTROLLED STUDY; CYTOTOXICITY; ELECTROSPINNING; EPITHELIZATION; HUMAN; HUMAN CELL; HYDROPHILICITY; IN VITRO STUDY; IN VIVO STUDY; MALE; NEW ZEALAND WHITE (RABBIT); NONHUMAN; OSTEOBLAST; PROTEIN SECRETION; SKIN DEFECT; SKIN TRANSPLANTATION; STEM CELL; THERAPY EFFECT; TISSUE ENGINEERING; UMBILICAL VEIN ENDOTHELIAL CELL; URINE DERIVED STEM CELL; WOUND HEALING; ANIMAL; ARTIFICIAL MEMBRANE; CELL MOTION; CHEMISTRY; CONDITIONED MEDIUM; CYTOLOGY; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; PHARMACOLOGY; RABBIT; ULTRASTRUCTURE; URINE; YOUNG ADULT;

ADULT; ANIMALS; BIOCOMPATIBLE MATERIALS; CELL MOVEMENT; CELL PROLIFERATION; CULTURE MEDIA, CONDITIONED; ENZYME-LINKED IMMUNOSORBENT ASSAY; GELATIN; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MEMBRANES, ARTIFICIAL; NANOFIBERS; NEOVASCULARIZATION, PHYSIOLOGIC; POLYESTERS; RABBITS; STEM CELLS; URINE; WOUND HEALING; YOUNG ADULT;

EID: 84907737224     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/s12967-014-0274-2     Document Type: Article

References (46)

1. Moise A, Constantinescu I, Serbanescu B, Gingu CV, Zamfirescu DG, Lascar I. Hand transplant:a challenge in immunological management of patients. J Med Life 2011, 4:287-290. 22567053.
2. Hautz T, Zelger B, Grahammer J, Krapf C, Amberger A, Brandacher G, Landin L, Müller H, Schön M, Cavadas P. Molecular markers and targeted therapy of skin rejection in composite tissue allotransplantation. Am J Transplant 2010, 10:1200-1209. 10.1111/j.1600-6143.2010.03075.x, 20353468.
3. Kanitakis J, Petruzzo P, Jullien D, Badet L, Dezza MC, Claudy A, Lanzetta M, Hakim N, Owen E, Dubernard J-M. Pathological score for the evaluation of allograft rejection in human hand (composite tissue) allotransplantation. Eur J Dermatol 2005, 15:235-238. 16048749.
4. Catalano E, Cochis A, Varoni E, Rimondini L, Azzimonti B. Tissue-engineered skin substitutes: an overview. J Artif Organs 2013, 16:397-403. 10.1007/s10047-013-0734-0, 24096542.
5. Pajardi G, Rapisarda V, Somalvico F, Scotti A, Russo GL, Ciancio F, Sgrò A, Nebuloni M, Allevi R, Torre ML: Skin substitutes based on allogenic fibroblasts or keratinocytes for chronic wounds not responding to conventional therapy: a retrospective observational study.Int Wound J 2014, in press.
6. Boa O, Cloutier CB, Genest H, Labbé R, Rodrigue B, Soucy J, Roy M, Arsenault F, Ospina CE, Dubé N. Prospective study on the treatment of lower-extremity chronic venous and mixed ulcers using tissue-engineered skin substitute made by the self-assembly approach. Adv Skin Wound Care 2013, 26:400-409. 10.1097/01.ASW.0000433102.48268.2a, 23958872.
7. Rodrigues C, de Assis AM, Moura DJ, Halmenschlager G, Saffi J, Xavier LL, da Cruz Fernandes M, Wink MR. New therapy of skin repair combining adipose-derived mesenchymal stem cells with sodium carboxymethylcellulose scaffold in a Pre-clinical Rat model. PLoS One 2014, 9:e96241. 10.1371/journal.pone.0096241, 24788779.
8. Machula H, Ensley B, Kellar R. Electrospun tropoelastin for delivery of therapeutic adipose-derived stem cells to full-thickness dermal wounds. Adv Wound Care 2014, 3:367-375. 10.1089/wound.2013.0513.
9. Lang R, Liu G, Shi Y, Bharadwaj S, Leng X, Zhou X, Liu H, Atala A, Zhang Y. Self-renewal and differentiation capacity of urine-derived stem cells after urine preservation for 24 hours. PLoS One 2013, 8:e53980. 10.1371/journal.pone.0053980, 23349776.
10. Zhang Y, McNeill E, Tian H, Soker S, Andersson K-E, Yoo JJ, Atala A. Urine derived cells are a potential source for urological tissue reconstruction. J Urol 2008, 180:2226-2233. 10.1016/j.juro.2008.07.023, 18804817.
11. Bodin A, Bharadwaj S, Wu S, Gatenholm P, Atala A, Zhang Y. Tissue-engineered conduit using urine-derived stem cells seeded bacterial cellulose polymer in urinary reconstruction and diversion. Biomaterials 2010, 31:8889-8901. 10.1016/j.biomaterials.2010.07.108, 20800278.
12. Bharadwaj S, Liu G, Shi Y, Wu R, Yang B, He T, Fan Y, Lu X, Zhou X, Liu H. Multipotential differentiation of human urine-derived stem cells: Potential for therapeutic applications in urology. Stem Cells 2013, 31:1840-1856. 10.1002/stem.1424, 23666768.
13. Wu S, Wang Z, Bharadwaj S, Hodges SJ, Atala A, Zhang Y. Implantation of autologous urine derived stem cells expressing vascular endothelial growth factor for potential use in genitourinary reconstruction. J Urol 2011, 186:640-647. 10.1016/j.juro.2011.03.152, 21683398.
14. Guan J-J, Niu X, Gong F-X, Hu B, Guo S-C, Lou Y-L, Zhang C-Q, Deng Z-F, Wang Y. Biological characteristics of human-urine-derived stem cells: potential for cell-based therapy in neurology. Tissue Eng Part A 2014, 20:1794-1806. 10.1089/ten.tea.2013.0584, 24387670.
15. Chai C, Leong KW. Biomaterials approach to expand and direct differentiation of stem cells. Mol Ther 2007, 15:467-480. 10.1038/sj.mt.6300084, 17264853.
16. Li WJ, Laurencin CT, Caterson EJ, Tuan RS, Ko FK. Electrospun nanofibrous structure: a novel scaffold for tissue engineering. J Biomed Mater Res 2002, 60:613-621. 10.1002/jbm.10167, 11948520.
17. Li D, Xia Y. Electrospinning of nanofibers: reinventing the wheel?. Adv Mater 2004, 16:1151-1170. 10.1002/adma.200400719.
18. Nie H, He A, Jia B, Wang F, Jiang Q, Han CC. A novel carrier of radionuclide based on surface modified poly (lactide- < i > co -glycolide) nanofibrous membrane. Polymer 2010, 51:3344-3348. 10.1016/j.polymer.2010.05.014.
19. Greiner A, Wendorff JH. Electrospinning: a fascinating method for the preparation of ultrathin fibers. Angew Chem Int Ed 2007, 46:5670-5703. 10.1002/anie.200604646.
20. Alvarez-Perez MA, Guarino V, Cirillo V, Ambrosio L. Influence of gelatin cues in PCL electrospun membranes on nerve outgrowth. Biomacromolecules 2010, 11:2238-2246. 10.1021/bm100221h, 20690634.
21. Zhang Y, Venugopal J, Huang Z-M, Lim C, Ramakrishna S. Characterization of the surface biocompatibility of the electrospun PCL-collagen nanofibers using fibroblasts. Biomacromolecules 2005, 6:2583-2589. 10.1021/bm050314k, 16153095.
22. Zhou Z, Zhou Y, Chen Y, Nie H, Wang Y, Li F, Zheng Y. Bilayer porous scaffold based on poly-(e{open}-caprolactone) nanofibrous membrane and gelatin sponge for favoring cell proliferation. Appl Surf Sci 2011, 258:1670-1676. 10.1016/j.apsusc.2011.09.120.
23. Zhang Y, Ouyang H, Lim CT, Ramakrishna S, Huang ZM. Electrospinning of gelatin fibers and gelatin/PCL composite fibrous scaffolds. J Biomed Mater Res B Appl Biomater 2005, 72:156-165. 10.1002/jbm.b.30128, 15389493.
24. Hartman O, Zhang C, Adams EL, Farach-Carson MC, Petrelli NJ, Chase BD, Rabolt JF. Biofunctionalization of electrospun PCL-based scaffolds with perlecan domain IV peptide to create a 3-D pharmacokinetic cancer model. Biomaterials 2010, 31:5700-5718. 10.1016/j.biomaterials.2010.03.017, 20417554.
25. Hajiali H, Shahgasempour S, Naimi-Jamal MR, Peirovi H. Electrospun PGA/gelatin nanofibrous scaffolds and their potential application in vascular tissue engineering. Int J Nanomedicine 2011, 6:2133. 10.2147/IJN.S24312, 22114477.
26. Chong E, Phan T, Lim I, Zhang Y, Bay B, Ramakrishna S, Lim C. Evaluation of electrospun PCL/gelatin nanofibrous scaffold for wound healing and layered dermal reconstitution. Acta Biomater 2007, 3:321-330. 10.1016/j.actbio.2007.01.002, 17321811.
27. Ghasemi-Mobarakeh L, Prabhakaran MP, Morshed M, Nasr-Esfahani M-H, Ramakrishna S. Electrospun poly(e{open}-caprolactone)/gelatin nanofibrous scaffolds for nerve tissue engineering. Biomaterials 2008, 29:4532-4539. 10.1016/j.biomaterials.2008.08.007, 18757094.
28. Revi D, Paul W, Anilkumar T, Sharma CP: Chitosan scaffold co-cultured with keratinocyte and fibroblast heals full thickness skin wounds in rabbit.J Biomed Mater Res A 2013, in press.
29. Jacobi J, Jang JJ, Sundram U, Dayoub H, Fajardo LF, Cooke JP. Nicotine accelerates angiogenesis and wound healing in genetically diabetic mice. Am J Pathol 2002, 161:97-104. 10.1016/S0002-9440(10)64161-2, 12107094.
30. Galeano M, Altavilla D, Cucinotta D, Russo GT, Calò M, Bitto A, Marini H, Marini R, Adamo EB, Seminara P. Recombinant human erythropoietin stimulates angiogenesis and wound healing in the genetically diabetic mouse. Diabetes 2004, 53:2509-2517. 10.2337/diabetes.53.9.2509, 15331568.
31. Yoon Y-S, Murayama T, Gravereaux E, Tkebuchava T, Silver M, Curry C, Wecker A, Kirchmair R, Hu CS, Kearney M. VEGF-C gene therapy augments postnatal lymphangiogenesis and ameliorates secondary lymphedema. J Clin Invest 2003, 111:717-725. 10.1172/JCI15830, 12618526.
32. Hamano Y, Zeisberg M, Sugimoto H, Lively JC, Maeshima Y, Yang C, Hynes RO, Werb Z, Sudhakar A, Kalluri R. Physiological levels of tumstatin, a fragment of collagen IV α3 chain, are generated by MMP-9 proteolysis and suppress angiogenesis via αVβ3 integrin. Cancer Cell 2003, 3:589-601. 10.1016/S1535-6108(03)00133-8, 12842087.
33. Jurmeister S, Baumann M, Balwierz A, Keklikoglou I, Ward A, Uhlmann S, Zhang JD, Wiemann S, Sahin T. MicroRNA-200c represses migration and invasion of breast cancer cells by targeting actin-regulatory proteins FHOD1 and PPM1F. Mol Cell Biol 2012, 32:633-651. 10.1128/MCB.06212-11, 22144583.
34. Pang H, Flinn R, Patsialou A, Wyckoff J, Roussos ET, Wu H, Pozzuto M, Goswami S, Condeelis JS, Bresnick AR. Differential enhancement of breast cancer cell motility and metastasis by helical and kinase domain mutations of class IA phosphoinositide 3-kinase. Cancer Res 2009, 69:8868-8876. 10.1158/0008-5472.CAN-09-1968, 19903845.
35. Martin P. Wound healing-aiming for perfect skin regeneration. Science 1997, 276:75-81. 10.1126/science.276.5309.75, 9082989.
36. Liang X, Boppart SA. Biomechanical properties of in vivo human skin from dynamic optical coherence elastography. Biomed Eng IEEE Trans on 2010, 57:953-959. 10.1109/TBME.2009.2033464.
37. Falanga V. Wound healing and its impairment in the diabetic foot. Lancet 2005, 366:1736-1743. 10.1016/S0140-6736(05)67700-8, 16291068.
38. Epstein FH, Singer AJ, Clark RA. Cutaneous wound healing. New Engl J Med 1999, 341:738-746. 10.1056/NEJM199909023411006.
39. Kim JW, Lee JH, Lyoo YS, Jung DI, Park HM. The effects of topical mesenchymal stem cell transplantation in canine experimental cutaneous wounds. Vet Dermatol 2013, 24:e242-e253. 10.1111/vde.12011.
40. Wu Y, Chen L, Scott PG, Tredget EE. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells 2007, 25:2648-2659. 10.1634/stemcells.2007-0226, 17615264.
41. Bharadwaj S, Liu G, Shi Y, Markert C, Andersson K-E, Atala A, Zhang Y. Characterization of urine-derived stem cells obtained from upper urinary tract for use in cell-based urological tissue engineering. Tissue Eng Part A 2011, 17:2123-2132. 10.1089/ten.tea.2010.0637, 21513463.
42. Wu S, Liu Y, Bharadwaj S, Atala A, Zhang Y. Human urine-derived stem cells seeded in a modified 3D porous small intestinal submucosa scaffold for urethral tissue engineering. Biomaterials 2011, 32:1317-1326. 10.1016/j.biomaterials.2010.10.006, 21055807.
43. Hofmann M, Wollert KC, Meyer GP, Menke A, Arseniev L, Hertenstein B, Ganser A, Knapp WH, Drexler H. Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 2005, 111:2198-2202. 10.1161/01.CIR.0000163546.27639.AA, 15851598.
44. Arnold F, West DC. Angiogenesis in wound healing. Pharmacol Ther 1991, 52:407-422. 10.1016/0163-7258(91)90034-J, 1726477.
45. Chen L, Tredget EE, Wu PY, Wu Y. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 2008, 3:e1886. 10.1371/journal.pone.0001886, 18382669.
46. Sachewsky N, Hunt J, Cooke MJ, Azimi A, Zarin T, Miu C, Shoichet MS, Morshead CM. Cyclosporin A enhances neural precursor cell survival in mice through a calcineurin-independent pathway. Dis Model Mech 2014, 7:953-961. 10.1242/dmm.014480, 25056698.