Layer-by-layer paper-stacking nanofibrous membranes to deliver adipose-derived stem cells for bone regeneration

International Journal of Nanomedicine

Volumn 10, Issue , 2015, Pages 1273-1290

  Wan, Wenbing ^a,c   Zhang, Shiwen ^b,d   Ge, Liangpeng ^b,c,e   Li, Qingtao ^a   Fang, Xingxing ^a   Yuan, Quan ^d   Zhong, Wen ^b   Ouyang, Jun ^a   Xing, Malcolm ^a,b  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF MANITOBA   (Canada)

^c Manitoba Institute of Child Health   (Canada)

^d SICHUAN UNIVERSITY   (China)

^e Chongqing Academy of Animal Sciences   (China)

Author keywords

Adipose derived stem cells; Bone regeneration; Calvarial defect; Layer by layer membrane; Paper stacking

Indexed keywords

ALPHA4 INTEGRIN; BETA1 INTEGRIN; BONE SIALOPROTEIN; GELATIN; OSTEOCALCIN; OSTEOPONTIN; OSTEOPROTEGERIN; POLYCAPROLACTONE; THY 1 ANTIGEN; TRANSCRIPTION FACTOR OSTERIX; TRANSCRIPTION FACTOR RUNX2; ARTIFICIAL MEMBRANE; BIOMATERIAL; NANOFIBER;

ADIPOSE DERIVED STEM CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL MEMBRANE; BIOCOMPATIBILITY; BONE DENSITY; BONE DEVELOPMENT; BONE REGENERATION; CELL DIFFERENTIATION; CELL INTERACTION; CELL VIABILITY; CONTROLLED STUDY; CROSS LINKING; DEVICE INFECTION; ELECTROSPINNING; FLOW CYTOMETRY; GENE EXPRESSION; HISTOLOGY; IN VITRO STUDY; IN VIVO STUDY; LAYER BY LAYER PAPER STACKING; LAYER BY LAYER PAPER STACKING MEMBRANE SCAFFOLD; MALE; MICRO-COMPUTED TOMOGRAPHY; NANOFABRICATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKULL DEFECT; STEM CELL TRANSPLANTATION; SURGICAL MESH; TISSUE SCAFFOLD; ADIPOCYTE; ANIMAL; CELL CULTURE; CHEMISTRY; DRUG EFFECTS; METABOLISM; PROCEDURES; STEM CELL; TISSUE ENGINEERING;

RATTUS;

ADIPOCYTES; ANIMALS; BIOCOMPATIBLE MATERIALS; BONE REGENERATION; CELL DIFFERENTIATION; CELLS, CULTURED; MEMBRANES, ARTIFICIAL; NANOFIBERS; OSTEOGENESIS; RATS; STEM CELLS; TISSUE ENGINEERING;

EID: 84922990641     PISSN: 11769114     EISSN: 11782013     Source Type: Journal    
DOI: 10.2147/IJN.S77118     Document Type: Article

References (66)

1. Petite H, Viateau V, Bensaid W, et al. Tissue-engineered bone regeneration. Nat Biotech. 2000;18:959–963.
2. Wang H, Li Y, Zuo Y, Li J, Ma S, Cheng L. Biocompatibility and osteogenesis of biomimetic nano-hydroxyapatite/polyamide composite scaffolds for bone tissue engineering. Biomaterials. 2007;28:3338–2348.
3. Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotech. 2005;23:47–55.
4. Kim SS, Sun Park M, Jeon O, Yong Choi C, Kim BS. Poly(lactide-co-glycolide)/hydroxyapatite composite scaffolds for bone tissue engineering. Biomaterials. 2006;27:1399–1409.
5. Eng G, Lee BW, Parsa H, et al. Assembly of complex cell microenvironments using geometrically docked hydrogel shapes. Proc Natl Acad Sci U S A. 2013;110:4551–4556.
6. Khetan S, Burdick JA. Patterning network structure to spatially control cellular remodeling and stem cell fate within 3-dimensional hydrogels. Biomaterials. 2010;31:8228–8834.
7. Derda R, Laromaine A, Mammoto A, et al. Paper-supported 3D cell culture for tissue-based bioassays. Proc Natl Acad Sci U S A. 2009;106:18457–18462.
8. Pampaloni F, Reynaud EG, Stelzer EHK. The third dimension bridges the gap between cell culture and live tissue. Nat Rev Mol Cell Biol. 2007;8:839–845.
9. Griffith LG, Swartz MA. Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol. 2006;7:211–224.
10. Yamada KM, Cukierman E. Modeling tissue morphogenesis and cancer in 3D. Cell. 2007;130:601–610.
11. Costa RR, Custodio CA, Arias FJ, Rodriguez-Cabello JC, Mano JF. Layer-by-layer assembly of chitosan and recombinant biopolymers into biomimetic coatings with multiple stimuli-responsive properties. Small. 2011;7:2640–2649.
12. Cui L, Liu B, Liu G, et al. Repair of cranial bone defects with adipose derived stem cells and coral scaffold in a canine model. Biomaterials. 2007;28:5477–5486.
13. Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res. 2007;100:1249–1260.
14. Liu G, Zhang Y, Liu B, Sun J, Li W, Cui L. Bone regeneration in a canine cranial model using allogeneic adipose derived stem cells and coral scaffold. Biomaterials. 2013;34:2655–2664.
15. Lin CY, Lin KJ, Kao CY, et al. The role of adipose-derived stem cells engineered with the persistently expressing hybrid baculovirus in the healing of massive bone defects. Biomaterials. 2011;32:6505–6614.
16. Frohbergh ME, Katsman A, Botta GP, et al. Electrospun hydroxyapatite-containing chitosan nanofibers crosslinked with genipin for bone tissue engineering. Biomaterials. 2012;33:9167–9178.
17. Liu W, Thomopoulos S, Xia Y. Electrospun nanofibers for regenerative medicine. Adv Healthc Mater. 2012;1:10–25.
18. Alamein MA, Liu Q, Stephens S, et al. Nanospiderwebs: artificial 3D extracellular matrix from nanofibers by novel clinical grade electrospinning for stem cell delivery. Adv Healthc Mater. 2013;2:702–717.
19. Orive G, Santos E, Pedraz JL, Hernandez RM. Application of cell encapsulation for controlled delivery of biological therapeutics. Adv Drug Deliv Rev. 2014;67–8:3–14.
20. Fischbach C, Chen R, Matsumoto T, et al. Engineering tumors with 3D scaffolds. Nat Meth. 2007;4:855–860.
21. Zhang H, Lin CY, Hollister SJ. The interaction between bone marrow stromal cells and RGD-modified three-dimensional porous polycaprolactone scaffolds. Biomaterials. 2009;30:4063–4069.
22. Di Maggio N, Piccinini E, Jaworski M, Trumpp A, Wendt DJ, Martin I. Toward modeling the bone marrow niche using scaffold-based 3D culture systems. Biomaterials. 2011;32:321–329.
23. Kumar G, Tison CK, Chatterjee K, et al. The determination of stem cell fate by 3D scaffold structures through the control of cell shape. Biomaterials. 2011;32:9188–9196.
24. Levenberg S, Huang NF, Lavik E, Rogers AB, Itskovitz-Eldor J, Langer R. Differentiation of human embryonic stem cells on three-dimensional polymer scaffolds. Proc Natl Acad Sci U S A. 2003;100:12741–12746.
25. Cowan CM, Shi YY, Aalami OO, et al. Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nat Biotechnol. 2004;22:560–7.
26. Frohlich M, Gimble JM, Grayson WL, Kregar-Velikonja N, Marolt D, Vunjak-Novakovic G. Bone grafts engineered from human adipose-derived stem cells in perfusion bioreactor culture. Tissue Eng Part A. 2010;16:179.
27. Young DA, Choi YS, Engler AJ, Christman KL. Stimulation of adipogenesis of adult adipose-derived stem cells using substrates that mimic the stiffness of adipose tissue. Biomaterials. 2013;34:8581–8588.
28. Katsuda T, Tsuchiya R, Kosaka N, et al. Human adipose tissue-derived mesenchymal stem cells secrete functional neprilysin-bound exosomes. Sci Rep. 2013;3:1197.
29. Estes BT, Diekman BO, Gimble JM, Guilak F. Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype. Nat Protoc. 2010;5:1294–1311.
30. Ji W, Yang F, Ma J, et al. Incorporation of stromal cell-derived factor-1alpha in PCL/gelatin electrospun membranes for guided bone regeneration. Biomaterials. 2013;34:735–745.
31. Lee J, Yoo JJ, Atala A, Lee SJ. The effect of controlled release of PDGF-BB from heparin-conjugated electrospun PCL/gelatin scaffolds on cellular bioactivity and infiltration. Biomaterials. 2012;33:6709–6720.
32. Xue J, He M, Liu H, et al. Drug loaded homogeneous electrospun PCL/gelatin hybrid nanofiber structures for anti-infective tissue regeneration membranes. Biomaterials. 2014;35:9395–9405.
33. Bigi A, Panzavolta S, Rubini K. Relationship between triple-helix content and mechanical properties of gelatin films. Biomaterials. 2004;25:5675–5680.
34. Xue J, Feng B, Zheng R, et al. Engineering ear-shaped cartilage using electrospun fibrous membranes of gelatin/polycaprolactone. Biomaterials. 2013;34:2624–2631.
35. Zhao Y, Lin H, Zhang J, et al. Crosslinked three-dimensional demineralized bone matrix for the adipose-derived stromal cell proliferation and differentiation. Tissue Eng Part A. 2009;15:13–21.
36. Haraguchi Y, Shimizu T, Sasagawa T, et al. Fabrication of functional three-dimensional tissues by stacking cell sheets in vitro. Nat Protoc. 2012;7:850–858.
37. Benesch J, Mano JF, Reis RL. Proteins and their peptide motifs in acellular apatite mineralization of scaffolds for tissue engineering. Tissue Eng Part B Rev. 2008;14:433–445.
38. Spicer PP, Kretlow JD, Young S, Jansen JA, Kasper FK, Mikos AG. Evaluation of bone regeneration using the rat critical size calvarial defect. Nat Protoc. 2012;7:1918–1929.
39. Degano IR, Vilalta M, Bago JR, et al. Bioluminescence imaging of calvarial bone repair using bone marrow and adipose tissue-derived mesenchymal stem cells. Biomaterials. 2008;29:427–437.
40. Pieri F, Lucarelli E, Corinaldesi G, et al. Dose-dependent effect of adipose-derived adult stem cells on vertical bone regeneration in rabbit calvarium. Biomaterials. 2010;31:3527–3535.
41. Declercq HA, De Caluwe T, Krysko O, Bachert C, Cornelissen MJ. Bone grafts engineered from human adipose-derived stem cells in dynamic 3D-environments. Biomaterials. 2013;34:1004–1017.
42. Li W-J, 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.
43. Langer R, Vacanti JP. Tissue engineering. Science. 1993;260:920–926.
44. Awad HA, Wickham MQ, Leddy HA, Gimble JM, Guilak F. Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials. 2004;25:3211–3222.
45. Wang H, Hansen MB, Lowik DW, et al. Oppositely charged gelatin nanospheres as building blocks for injectable and biodegradable gels. Adv Mater. 2011;23:H119–H124.
46. Loverde SM, Klein ML, Discher DE. Nanoparticle shape improves delivery: rational coarse grain molecular dynamics (rCG-MD) of taxol in worm-like PEG-PCL micelles. Adv Mater. 2012;24:3823–3830.
47. Badami AS, Kreke MR, Thompson MS, Riffle JS, Goldstein AS. Effect of fiber diameter on spreading, proliferation, and differentiation of osteoblastic cells on electrospun poly(lactic acid) substrates. Biomaterials. 2006;27:596–606.
48. Liang D, Hsiao BS, Chu B. Functional electrospun nanofibrous scaffolds for biomedical applications. Adv Drug Deliv Rev. 2007;59:1392–1412.
49. Murakami T, Saito A, Hino S-i, et al. Signalling mediated by the endoplasmic reticulum stress transducer OASIS is involved in bone formation. Nat Cell Biol. 2009;11:1205–1211.
50. Mendonca G, Mendonca DB, Simoes LG, et al. The effects of implant surface nanoscale features on osteoblast-specific gene expression. Biomaterials. 2009;30:4053–4062.
51. Weilbaecher KN, Guise TA, McCauley LK. Cancer to bone: a fatal attraction. Nat Rev Cancer. 2011;11:411–425.
52. Opsahl Vital S, Gaucher C, Bardet C, et al. Tooth dentin defects reflect genetic disorders affecting bone mineralization. Bone. 2012;50:989–997.
53. Smith LB, Saunders PT. The skeleton: the new controller of male fertility? Cell. 2011;144:642–643.
54. Fulzele K, Riddle RC, DiGirolamo DJ, et al. Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell. 2010;142:309–319.
55. Ferron M, Wei J, Yoshizawa T, et al. Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell. 2010;142:296–308.
56. Simonet WS, Lacey DL, Dunstan CR, et al. Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell. 1997;89:309–319.
57. Matsubara H, Hogan DE, Morgan EF, Mortlock DP, Einhorn TA, Gerstenfeld LC. Vascular tissues are a primary source of BMP2 expression during bone formation induced by distraction osteogenesis. Bone. 2012;51:168–180.
58. Ye JH, Xu YJ, Gao J, et al. Critical-size calvarial bone defects healing in a mouse model with silk scaffolds and SATB2-modified iPSCs. Biomaterials. 2011;32:5065–5076.
59. Hamann C, Kirschner S, Gunther K-P, Hofbauer LC. Bone, sweet bone – osteoporotic fractures in diabetes mellitus. Nat Rev Endocrinol. 2012;8:297–305.
60. Giuliani N, Colla S, Morandi F, et al. Myeloma cells block RUNX2/CBFA1 activity in human bone marrow osteoblast progenitors and inhibit osteoblast formation and differentiation. Blood. 2005;106:2472–2483.
61. Shi J, Ouyang J, Li Q, Wang L, Wu J, Zhong W, Xing MM. Cell-compatible hydrogels based on a multifunctional crosslinker with tunable stiffness for tissue engineering. J of Mater Chem. 2012;22:23952–23962.
62. Chen J, Qiu X, Wang L, Zhong W, Kong J, Xing MM. Free-Standing Cell Sheet Assembled with Ultrathin Extracellular Matrix as an Innovative Approach for Biomimetic Tissues. Adv Funct Mater. 2014;24(15):2216–2223.
63. Chen J, Zhou B, Li Q, Ouyang J, Kong J, Zhong W, Xing MM. PLLA-PEG-TCH-labeled bioactive molecule nanofibers for tissue engineering. Int J Nanomedicine. 2011;6:2533–2542.
64. Wang Z, Xing M, Ojo O. Mussel-inspired ultrathin film on oxidized Ti–6Al–4V surface for enhanced BMSC activities and antibacterial capability. RSC Adv. 2014;4:55790–55799.
65. Li X, Zhou J, Liu Z, Chen J, Lü S, Sun H, et al. A PNIPAAm-based thermosensitive hydrogel containing SWCNTs for stem cell transplantation in myocardial repair. Biomaterials. 2014;35(22):5679–5688.
66. Ge L, Li Q, Huang Y, Yang S, et al. Polydopamine-coated paper-stack nanofibrous membranes enhancing adipose stem cells’ adhesion and osteogenic differentiation. J Mater Chem B. 2014;2:6917–6923.