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Recellularization of decellularized human adipose-tissue-derived extracellular matrix sheets with other human cell types

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Abstract

Decellularized human extracellular matrices (ECMs) are an extremely appealing biomaterial for tissue engineering and regenerative medicine. In this study, we decellularized human adipose tissue, fabricated a thin ECM sheet and explored the potential of this human adipose-derived ECM sheet as a substrate to support the formation of tissues other than adipose tissue. Acellular ECM sheets were fabricated from human adipose tissue through successive physical and chemical treatments: homogenization, centrifugation, casting, freeze-drying and sodium dodecyl sulfate treatment. The ECM sheets exhibited good mechanical properties, despite their porous structure. They degraded quickly in the presence of collagenase and the degradation rate increased with the collagenase concentration in phosphate-buffered saline. Five different human cell types, covering a broad range of cells and applications (normal human dermal fibroblasts, human aortic smooth muscle cells, human chondrocytes, human umbilical vein endothelial cells and human adipose-derived stem cells), were seeded onto the ECM sheets. All the human cell types spread well, proliferated and were successfully integrated into the decellularized ECM sheet. Overall, the results suggest that recellularized ECM sheets are a promising substitute for defective or damaged human tissues.

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References

  • Abdull Rasad MSB, Halim AS, Hashim K, Rashid AHA, Yusof N, Shamsuddin S (2010) In vitro evaluation of novel chitosan derivatives sheet and paste cytocompatibility on human dermal fibroblasts. Carbohydr Polym 79:1094–1100

    Article  CAS  Google Scholar 

  • Badylak SF, Freytes DO, Gilbert TW (2009) Extracellular matrix as a biological scaffold material: structure and function. Acta Biomater 5:1–13

    Article  PubMed  CAS  Google Scholar 

  • Beatty MW, Ojha AK, Cook JL, Alberts LR, Mahanna GK, Iwasaki LR, Nickel JC (2002) Small intestinal submucosa versus salt-extracted polyglycolic acid-poly-L-lactic acid: a comparison of neocartilage formed in two scaffold materials. Tissue Eng 8:955–968

    Article  PubMed  CAS  Google Scholar 

  • Borschel GH, Dennis RG, Kuzon WM Jr (2004) Contractile skeletal muscle tissue-engineered on an acellular scaffold. Plast Reconstr Surg 113:595–602

    Article  PubMed  Google Scholar 

  • Boyce ST (2001) Design principles for composition and performance of cultured skin substitutes. Burns 27:523–533

    Article  PubMed  CAS  Google Scholar 

  • Choi JS, Yang HJ, Kim BS, Kim JD, Kim JY, Yoo B, Park K, Lee HY, Cho YW (2009) Human extracellular matrix (ECM) powders for injectable cell delivery and adipose tissue engineering. J Control Release 139:2–7

    Article  PubMed  CAS  Google Scholar 

  • Choi JS, Yang HJ, Kim BS, Kim JD, Lee SH, Lee EK, Park K, Cho YW, Lee HY (2010) Fabrication of porous extracellular matrix scaffolds from human adipose tissue. Tissue Eng Part C 16:387–396

    Article  CAS  Google Scholar 

  • Choi JS, Kim BS, Kim JY, Kim JD, Choi YC, Yang HJ, Park K, Lee HY, Cho YW (2011) Decellularized extracellular matrix derived from human adipose tissue as a potential scaffold for allograft tissue engineering. J Biomed Mater Res A 97:292–299

    PubMed  Google Scholar 

  • Cimini M, Boughner DR, Ronald JA, Johnston DE, Rogers KA (2005) Dermal fibroblasts cultured on small intestinal submucosa: conditions for the formation of a neotissue. J Biomed Mater Res A 75:895–906

    PubMed  Google Scholar 

  • Cuono C, Langdon R, McGuire J (1986) Use of cultured epidermal autografts and dermal allografts as skin replacement after burn injury. Lancet 1:1123–1124

    Article  PubMed  CAS  Google Scholar 

  • Dahms SE, Piechota HJ, Dahiya R, Lue TF, Tanagho EA (1998) Composition and biomechanical properties of the bladder acellular matrix graft: comparative analysis in rat, pig and human. Br J Urol 82:411–419

    Article  PubMed  CAS  Google Scholar 

  • De Cock LJ, De Koker S, De Vos F, Vervaet C, Remon JP, De Geest BG (2010) Layer-by-layer incorporation of growth factors in decellularized aortic heart valve leaflets. Biomacromolecules 11:1002–1008

    Article  PubMed  Google Scholar 

  • Du C, Cui FZ, Zhu XD, De Groot K (1999) Three-dimensional nano-HAp/collagen matrix loading with osteogenic cells in organ culture. J Biomed Mater Res 44:407–415

    Article  PubMed  CAS  Google Scholar 

  • Ellis MJ, Chaudhuri JB (2008) Human bone derived cell culture on PLGA flat sheet membranes of different lactide:glycolide ratio. Biotechnol Bioeng 101:369–377

    Article  PubMed  CAS  Google Scholar 

  • Finne-Wistrand A, Albertsson AC, Kwon OH, Kawazoe N, Chen G, Kang IK, Hasuda H, Gong J, Ito Y (2008) Resorbable scaffolds from three different techniques: electrospun fabrics, salt-leaching porous films and smooth flat surfaces. Macromol Biosci 8:951–959

    Article  PubMed  CAS  Google Scholar 

  • Hashizume H, Ushiki T (2002) Three-dimensional cytoarchitecture of angiogenic blood vessels in a gelatin sheet implanted in the rat skeletal muscular layers. Arch Histol Cytol 65:347–357

    Article  PubMed  Google Scholar 

  • Hutmacher DW (2001) Scaffold design and fabrication technologies for engineering tissues-state of the art and future perspectives. J Biomater Sci Polym Ed 12:107–124

    Article  PubMed  CAS  Google Scholar 

  • Ingram JH, Korossis S, Howling G, Fisher J, Ingham E (2007) The use of ultrasonication to aid recellularization of acellular natural tissue scaffolds for use in anterior cruciate ligament reconstruction. Tissue Eng 13:1561–1572

    Article  PubMed  CAS  Google Scholar 

  • Kim BS, Choi JS, Kim JD, Yeo TY, Cho YW (2010) Improvement of stem cell viability in hyaluronic acid hydrogels using dextran microspheres. J Biomater Sci Polym Ed 21:1701–1711

    Article  PubMed  CAS  Google Scholar 

  • Kuo YC, Ku IN (2008) Cartilage regeneration by novel polyethylene oxide/chitin/chitosan scaffolds. Biomacromolecules 9:2662–2669

    Article  PubMed  CAS  Google Scholar 

  • Kuroyanagi Y, Yamada N, Yamashita R, Uchinuma E (2001) Tissue-engineered product: allogeneic cultured dermal substitute composed of spongy collagen with fibroblasts. Artif Organs 25:180–186

    Article  PubMed  CAS  Google Scholar 

  • Lo H, Kadiyala S, Guggino SE, Leong KW (1996) Poly(L-lactic acid) foams with cell seeding and controlled-release capacity. J Biomed Mater Res 90:475–484

    Article  Google Scholar 

  • Malcarney HL, Bonar F, Murrell GA (2005) Early inflammatory reaction after rotator cuff repair with a porcine small intestine submucosal implant: a report of 4 cases. Am J Sports Med 33:907–911

    Article  PubMed  Google Scholar 

  • Midwood KS, Williams LV, Schwarzbauer JE (2004) Tissue repair and the dynamics of the extracellular matrix. Int J Biochem Cell Biol 36:1031–1037

    Article  PubMed  CAS  Google Scholar 

  • Mikos AG, Thorsen AJ, Czerwonka LA, Bao Y, Langer R, Winslow DN, Vacanti JP (1994) Preparation and characterization of poly(L-lactic acid) foams. Polymer 35:1068–1077

    Article  CAS  Google Scholar 

  • Mirsadraee S, Wilcox HE, Korossis SA, Kearney JN, Watterson KG, Fisher J, Ingham E (2006) Development and characterization of an acellular human pericardial matrix for tissue engineering. Tissue Eng 12:763–773

    Article  PubMed  CAS  Google Scholar 

  • Misseri R, Cain MP, Casale AJ, Kaefer M, Meldrum KK, Rink RC, Matthews R (2005) Small intestinal submucosa bladder neck slings for incontinence associated with neuropathic bladder. J Urol 174:1680–1682

    Article  PubMed  Google Scholar 

  • Mohan D, Melvin JW (1982) Failure properties of passive human aortic tissue. I. Uniaxial tension tests. J Biomech 15:887–902

    Article  PubMed  CAS  Google Scholar 

  • Nishimura T, Ueno T, Nakatsu H, Oga A, Kobayashi S, Oka M (2010) In vivo motility evaluation of the grafted gastric wall with small intestinal submucosa. Tissue Eng Part A 16:1761–1768

    Article  PubMed  Google Scholar 

  • Oiwa Y, Nakai K, Takayama M, Naka D, Itakura T (2004) Microvascular decompression of cranial nerves using sheets of a dural substitute-technical note. Neurol Med Chir 44:94–100

    Article  Google Scholar 

  • Piechota HJ, Gleason CA, Dahms SE, Dahiya R, Nunes LS, Lue TF, Tanagho EA (1999) Bladder acellular matrix graft: in vivo functional properties of the regenerated rat bladder. Urol Res 27:206–213

    Article  PubMed  CAS  Google Scholar 

  • Place ES, Evans ND, Stevens MM (2009) Complexity in biomaterials for tissue engineering. Nat Mater 8:457–470

    Article  PubMed  CAS  Google Scholar 

  • Schopka S, Schmid FX, Hirt S, Birnbaum DE, Schmid C, Lehle K (2009) Recellularization of biological heart valves with human vascular cells: in vitro hemocompatibility assessment. J Biomed Mater Res B Appl Biomater 88:130–138

    Google Scholar 

  • Shoichet MS (2010) Polymer scaffolds for biomaterials applications. Macromolecules 43:581–591

    Article  CAS  Google Scholar 

  • Sodian R, Hoerstrup SP, Sperling JS, Daebritz SH, Martin DP, Schoen FJ, Vacanti JP, Mayer JE Jr (2000) Tissue engineering of heart valves: in vitro experiences. Ann Thorac Surg 70:140–144

    Google Scholar 

  • Tsukihara H, Takamoto S, Kitahori K, Matsuda K, Murakami A, Novick RJ, Suematsu Y (2006) Prevention of postoperative pericardial adhesions with a novel regenerative collagen sheet. Ann Thorac Surg 81:650–657

    Article  PubMed  Google Scholar 

  • Tu Q, Zhang Y, Ge D, Wu J, Chen H (2008) Novel tissue-engineered vascular patches based on decellularized canine aortas and their recellularization in vitro. Appl Surf Sci 255:282–285

    Article  CAS  Google Scholar 

  • van Tienen TG, Heijkants RG, Buma P, de Groot JH, Pennings AJ, Veth RP (2002) Tissue ingrowth and degradation of two biodegradable porous polymers with different porosities and pore sizes. Biomaterials 23:1731–1738

    Google Scholar 

  • Voytik-Harbin SL, Brightman AO, Waisner BZ, Robinson JP, Lamar CH (1998) Small intestinal submucosa: a tissue-derived extracellular matrix that promotes tissue-specific growth and differentiation of cells in vitro. Tissue Eng 4:157–174

    Article  Google Scholar 

  • Wake MC, Patrick CW Jr, Mikos AG (1994) Pore morphology effects on the fibrovascular tissue growth in porous polymer substrates. Cell Transplant 3:339–343

    Google Scholar 

  • Whang K, Thomas CH, Healy KE, Nuber G (1995) A novel method to fabricate bioabsorbable scaffolds. Polymer 36:837–842

    Article  CAS  Google Scholar 

  • White JK, Agnihotri AK, Titus JS, Torchiana DF (2005) A stentless trileaflet valve from a sheet of decellularized porcine small intestinal submucosa. Ann Thorac Surg 80:704–707

    Article  PubMed  Google Scholar 

  • Yokoya S, Mochizuki Y, Nagata Y, Deie M, Ochi M (2008) Tendon-bone insertion repair and regeneration using polyglycolic acid sheet in the rabbit rotator cuff injury model. Am J Sports Med 36:1298–1309

    Article  PubMed  Google Scholar 

  • Zehr KJ, Yagubyan M, Connolly HM, Nelson SM, Schaff HV (2005) Aortic root replacement with a novel decellularized cryopreserved aortic homograft: postoperative immunoreactivity and early results. J Thorac Cardiovasc Surg 130:1010–1015

    Article  PubMed  Google Scholar 

  • Zhong S, Teo WE, Zhu X, Beuerman R, Ramakrishna S, Yung LY (2005) Formation of collagen-glycosaminoglycan blended nanofibrous scaffolds and their biological properties. Biomacromolecules 6:2998–3004

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Basic Science Research Program (grant no. 2009-0075546) and the Bio & Medical Technology Development Program (grant no. 2011-0019774) of the National Research Foundation of Korea (NRF) funded by the Korean government (MEST). Our research (grant no. 00046001) was also supported by Business for Academic-Industrial Cooperative Establishments funded by the Korea Small and Medium Business Administration in 2011.

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  1. Department of Chemical Engineering and Department of Bionanotechnology, Hanyang University, 1271 Sa-3 dong, Sangnok-gu, Ansan, Gyeonggi-do, 426-791, Republic of Korea

    Beob Soo Kim, Ji Suk Choi, Jae Dong Kim, Young Chan Choi & Yong Woo Cho

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  1. Beob Soo Kim
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  2. Ji Suk Choi
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  3. Jae Dong Kim
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Correspondence to Yong Woo Cho.

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Kim, B.S., Choi, J.S., Kim, J.D. et al. Recellularization of decellularized human adipose-tissue-derived extracellular matrix sheets with other human cell types. Cell Tissue Res 348, 559–567 (2012). https://doi.org/10.1007/s00441-012-1391-y

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