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Recent Advancements in Decellularized Matrix-Based Biomaterials for Musculoskeletal Tissue Regeneration

  • Hyunbum Kim
  • Yunhye Kim
  • Mona Fendereski
  • Nathaniel S. Hwang
  • Yongsung HwangEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1077)

Abstract

The native extracellular matrix (ECM) within different origins of tissues provides a dynamic microenvironment for regulating various cellular functions. Thus, recent regenerative medicine and tissue engineering approaches for modulating various stem cell functions and their contributions to tissue repair include the utilization of tissue-specific decellularized matrix-based biomaterials. Because of their unique capabilities to mimic native extracellular microenvironments based on their three-dimensional structures, biochemical compositions, and biological cues, decellularized matrix-based biomaterials have been recognized as an ideal platform for engineering an artificial stem cell niche. Herein, we describe the most commonly used decellularization methods and their potential applications in musculoskeletal tissue engineering.

Keywords

Decellularization Extracellular matrix (ECM) Biomaterials Scaffold Microenvironment Musculoskeletal tissue regeneration 

Notes

Acknowledgement

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2016K1A4A3914725) and partially supported by the Soonchunhyang University Research Fund.

References

  1. 1.
    Langer R (2000) Biomaterials in drug delivery and tissue engineering: one laboratory’s experience. Acc Chem Res 33(2):94–101CrossRefGoogle Scholar
  2. 2.
    Shin H, Jo S, Mikos AG (2003) Biomimetic materials for tissue engineering. Biomaterials 24(24):4353–4364CrossRefGoogle Scholar
  3. 3.
    Lutolf MP, Hubbell JA (2005) Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 23(1):47–55.  https://doi.org/10.1038/nbt1055 CrossRefGoogle Scholar
  4. 4.
    Tibbitt MW, Anseth KS (2009) Hydrogels as extracellular matrix mimics for 3D cell culture. Biotechnol Bioeng 103(4):655–663.  https://doi.org/10.1002/bit.22361 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Hwang NS, Varghese S, Zhang Z, Elisseeff J (2006) Chondrogenic differentiation of human embryonic stem cell-derived cells in arginine-glycine-aspartate-modified hydrogels. Tissue Eng 12(9):2695–2706.  https://doi.org/10.1089/ten.2006.12.2695 CrossRefPubMedGoogle Scholar
  6. 6.
    Kim H, Lee Y, Kim Y, Hwang Y, Hwang N (2017) Biomimetically reinforced polyvinyl alcohol-based hybrid scaffolds for cartilage tissue engineering. Polymers 9(12):655CrossRefGoogle Scholar
  7. 7.
    Hwang Y, Phadke A, Varghese S (2011) Engineered microenvironments for self-renewal and musculoskeletal differentiation of stem cells. Regen Med 6(4):505–524.  https://doi.org/10.2217/rme.11.38 CrossRefPubMedGoogle Scholar
  8. 8.
    Badylak SF, Freytes DO, Gilbert TW (2009) Extracellular matrix as a biological scaffold material: structure and function. Acta Biomater 5(1):1–13.  https://doi.org/10.1016/j.actbio.2008.09.013 CrossRefPubMedGoogle Scholar
  9. 9.
    Brown BN, Valentin JE, Stewart-Akers AM, McCabe GP, Badylak SF (2009) Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials 30(8):1482–1491.  https://doi.org/10.1016/j.biomaterials.2008.11.040 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Saldin LT, Cramer MC, Velankar SS, White LJ, Badylak SF (2017) Extracellular matrix hydrogels from decellularized tissues: structure and function. Acta Biomater 49:1–15.  https://doi.org/10.1016/j.actbio.2016.11.068 CrossRefGoogle Scholar
  11. 11.
    Dziki JL, Huleihel L, Scarritt ME, Badylak SF (2017) Extracellular matrix bioscaffolds as immunomodulatory biomaterials. Tissue Eng Part A 23(19–20):1152–1159.  https://doi.org/10.1089/ten.TEA.2016.0538 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Badylak SF, Taylor D, Uygun K (2011) Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. Annu Rev Biomed Eng 13:27–53.  https://doi.org/10.1146/annurev-bioeng-071910-124743 CrossRefPubMedGoogle Scholar
  13. 13.
    Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM, Netoff TI, Taylor DA (2008) Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med 14(2):213–221.  https://doi.org/10.1038/nm1684 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Zhang W, Zhu Y, Li J, Guo Q, Peng J, Liu S, Yang J, Wang Y (2016) Cell-derived extracellular matrix: basic characteristics and current applications in orthopedic tissue engineering. Tissue Eng Part B Rev 22(3):193–207.  https://doi.org/10.1089/ten.TEB.2015.0290 CrossRefPubMedGoogle Scholar
  15. 15.
    Cheng CW, Solorio LD, Alsberg E (2014) Decellularized tissue and cell-derived extracellular matrices as scaffolds for orthopaedic tissue engineering. Biotechnol Adv 32(2):462–484.  https://doi.org/10.1016/j.biotechadv.2013.12.012 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Spang MT, Christman KL (2018) Extracellular matrix hydrogel therapies: in vivo applications and development. Acta Biomater 68:1–14.  https://doi.org/10.1016/j.actbio.2017.12.019 CrossRefPubMedGoogle Scholar
  17. 17.
    Crapo PM, Gilbert TW, Badylak SF (2011) An overview of tissue and whole organ decellularization processes. Biomaterials 32(12):3233–3243.  https://doi.org/10.1016/j.biomaterials.2011.01.057 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Gilpin A, Yang Y (2017) Decellularization strategies for regenerative medicine: from processing techniques to applications. Biomed Res Int 2017:9831534.  https://doi.org/10.1155/2017/9831534 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Syed O, Walters NJ, Day RM, Kim HW, Knowles JC (2014) Evaluation of decellularization protocols for production of tubular small intestine submucosa scaffolds for use in oesophageal tissue engineering. Acta Biomater 10(12):5043–5054.  https://doi.org/10.1016/j.actbio.2014.08.024 CrossRefPubMedGoogle Scholar
  20. 20.
    Gorschewsky O, Puetz A, Riechert K, Klakow A, Becker R (2005) Quantitative analysis of biochemical characteristics of bone-patellar tendon-bone allografts. Biomed Mater Eng 15(6):403–411PubMedGoogle Scholar
  21. 21.
    Reing JE, Brown BN, Daly KA, Freund JM, Gilbert TW, Hsiong SX, Huber A, Kullas KE, Tottey S, Wolf MT, Badylak SF (2010) The effects of processing methods upon mechanical and biologic properties of porcine dermal extracellular matrix scaffolds. Biomaterials 31(33):8626–8633.  https://doi.org/10.1016/j.biomaterials.2010.07.083 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Heerklotz H (2008) Interactions of surfactants with lipid membranes. Q Rev Biophys 41(3–4):205–264.  https://doi.org/10.1017/S0033583508004721 CrossRefPubMedGoogle Scholar
  23. 23.
    Lumpkins SB, Pierre N, McFetridge PS (2008) A mechanical evaluation of three decellularization methods in the design of a xenogeneic scaffold for tissue engineering the temporomandibular joint disc. Acta Biomater 4(4):808–816.  https://doi.org/10.1016/j.actbio.2008.01.016 CrossRefPubMedGoogle Scholar
  24. 24.
    Nakayama KH, Batchelder CA, Lee CI, Tarantal AF (2010) Decellularized rhesus monkey kidney as a three-dimensional scaffold for renal tissue engineering. Tissue Eng Part A 16(7):2207–2216.  https://doi.org/10.1089/ten.TEA.2009.0602 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Uygun BE, Soto-Gutierrez A, Yagi H, Izamis ML, Guzzardi MA, Shulman C, Milwid J, Kobayashi N, Tilles A, Berthiaume F, Hertl M, Nahmias Y, Yarmush ML, Uygun K (2010) Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix. Nat Med 16(7):814–820.  https://doi.org/10.1038/nm.2170 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Gilpin SE, Ren X, Okamoto T, Guyette JP, Mou H, Rajagopal J, Mathisen DJ, Vacanti JP, Ott HC (2014) Enhanced lung epithelial specification of human induced pluripotent stem cells on decellularized lung matrix. Ann Thorac Surg 98(5):1721–1729.; discussion 9.  https://doi.org/10.1016/j.athoracsur.2014.05.080 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Petersen TH, Calle EA, Colehour MB, Niklason LE (2012) Matrix composition and mechanics of decellularized lung scaffolds. Cells Tissues Organs 195(3):222–231.  https://doi.org/10.1159/000324896 CrossRefPubMedGoogle Scholar
  28. 28.
    Keane TJ, Swinehart IT, Badylak SF (2015) Methods of tissue decellularization used for preparation of biologic scaffolds and in vivo relevance. Methods 84:25–34.  https://doi.org/10.1016/j.ymeth.2015.03.005 CrossRefGoogle Scholar
  29. 29.
    Fu Y, Fan X, Tian C, Luo J, Zhang Y, Deng L, Qin T, Lv Q (2016) Decellularization of porcine skeletal muscle extracellular matrix for the formulation of a matrix hydrogel: a preliminary study. J Cell Mol Med 20(4):740–749.  https://doi.org/10.1111/jcmm.12776 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Elder BD, Kim DH, Athanasiou KA (2010) Developing an articular cartilage decellularization process toward facet joint cartilage replacement. Neurosurgery 66(4):722–727.; discussion 7.  https://doi.org/10.1227/01.NEU.0000367616.49291.9F CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Petersen TH, Calle EA, Zhao L, Lee EJ, Gui L, Raredon MB, Gavrilov K, Yi T, Zhuang ZW, Breuer C, Herzog E, Niklason LE (2010) Tissue-engineered lungs for in vivo implantation. Science 329(5991):538–541.  https://doi.org/10.1126/science.1189345 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Flynn LE (2010) The use of decellularized adipose tissue to provide an inductive microenvironment for the adipogenic differentiation of human adipose-derived stem cells. Biomaterials 31(17):4715–4724.  https://doi.org/10.1016/j.biomaterials.2010.02.046 CrossRefPubMedGoogle Scholar
  33. 33.
    Xing Q, Yates K, Tahtinen M, Shearier E, Qian Z, Zhao F (2015) Decellularization of fibroblast cell sheets for natural extracellular matrix scaffold preparation. Tissue Eng Part C Methods 21(1):77–87.  https://doi.org/10.1089/ten.TEC.2013.0666 CrossRefPubMedGoogle Scholar
  34. 34.
    Lin P, Chan WC, Badylak SF, Bhatia SN (2004) Assessing porcine liver-derived biomatrix for hepatic tissue engineering. Tissue Eng 10(7–8):1046–1053.  https://doi.org/10.1089/ten.2004.10.1046 CrossRefPubMedGoogle Scholar
  35. 35.
    Funamoto S, Nam K, Kimura T, Murakoshi A, Hashimoto Y, Niwaya K, Kitamura S, Fujisato T, Kishida A (2010) The use of high-hydrostatic pressure treatment to decellularize blood vessels. Biomaterials 31(13):3590–3595.  https://doi.org/10.1016/j.biomaterials.2010.01.073 CrossRefPubMedGoogle Scholar
  36. 36.
    Sasaki S, Funamoto S, Hashimoto Y, Kimura T, Honda T, Hattori S, Kobayashi H, Kishida A, Mochizuki M (2009) In vivo evaluation of a novel scaffold for artificial corneas prepared by using ultrahigh hydrostatic pressure to decellularize porcine corneas. Mol Vis 15:2022–2028PubMedPubMedCentralGoogle Scholar
  37. 37.
    Seo Y, Jung Y, Kim SH (2018) Decellularized heart ECM hydrogel using supercritical carbon dioxide for improved angiogenesis. Acta Biomater 67:270–281.  https://doi.org/10.1016/j.actbio.2017.11.046 CrossRefPubMedGoogle Scholar
  38. 38.
    Halfwerk FR, Rouwkema J, Gossen JA, Grandjean JG (2018) Supercritical carbon dioxide decellularised pericardium: mechanical and structural characterisation for applications in cardio-thoracic surgery. J Mech Behav Biomed Mater 77:400–407.  https://doi.org/10.1016/j.jmbbm.2017.10.002 CrossRefPubMedGoogle Scholar
  39. 39.
    Calori GM, Mazza E, Colombo M, Ripamonti C (2011) The use of bone-graft substitutes in large bone defects: any specific needs? Injury 42(Suppl 2):S56–S63.  https://doi.org/10.1016/j.injury.2011.06.011 CrossRefPubMedGoogle Scholar
  40. 40.
    Lutolf MP, Weber FE, Schmoekel HG, Schense JC, Kohler T, Muller R, Hubbell JA (2003) Repair of bone defects using synthetic mimetics of collagenous extracellular matrices. Nat Biotechnol 21(5):513–518.  https://doi.org/10.1038/nbt818 CrossRefPubMedGoogle Scholar
  41. 41.
    Banwart JC, Asher MA, Hassanein RS (1995) Iliac crest bone graft harvest donor site morbidity. A statistical evaluation. Spine 20(9):1055–1060CrossRefGoogle Scholar
  42. 42.
    Phadke A, Hwang Y, Kim SH, Kim SH, Yamaguchi T, Masuda K, Varghese S (2013) Effect of scaffold microarchitecture on osteogenic differentiation of human mesenchymal stem cells. Eur Cell Mater 25:114–129CrossRefGoogle Scholar
  43. 43.
    Datta N, Holtorf HL, Sikavitsas VI, Jansen JA, Mikos AG (2005) Effect of bone extracellular matrix synthesized in vitro on the osteoblastic differentiation of marrow stromal cells. Biomaterials 26(9):971–977.  https://doi.org/10.1016/j.biomaterials.2004.04.001 CrossRefPubMedGoogle Scholar
  44. 44.
    Papadimitropoulos A, Scotti C, Bourgine P, Scherberich A, Martin I (2015) Engineered decellularized matrices to instruct bone regeneration processes. Bone 70:66–72.  https://doi.org/10.1016/j.bone.2014.09.007 CrossRefPubMedGoogle Scholar
  45. 45.
    Nyberg E, Rindone A, Dorafshar A, Grayson WL (2017) Comparison of 3D-printed poly-varepsilon-caprolactone scaffolds functionalized with tricalcium phosphate, hydroxyapatite, Bio-Oss, or decellularized bone matrix. Tissue Eng Part A 23(11–12):503–514.  https://doi.org/10.1089/ten.TEA.2016.0418 CrossRefPubMedGoogle Scholar
  46. 46.
    Gruskin E, Doll BA, Futrell FW, Schmitz JP, Hollinger JO (2012) Demineralized bone matrix in bone repair: history and use. Adv Drug Deliv Rev 64(12):1063–1077.  https://doi.org/10.1016/j.addr.2012.06.008 CrossRefPubMedGoogle Scholar
  47. 47.
    Lee DJ, Diachina S, Lee YT, Zhao L, Zou R, Tang N, Han H, Chen X, Ko CC (2016) Decellularized bone matrix grafts for calvaria regeneration. J Tissue Eng 7:2041731416680306.  https://doi.org/10.1177/2041731416680306 CrossRefGoogle Scholar
  48. 48.
    Hashimoto Y, Funamoto S, Kimura T, Nam K, Fujisato T, Kishida A (2011) The effect of decellularized bone/bone marrow produced by high-hydrostatic pressurization on the osteogenic differentiation of mesenchymal stem cells. Biomaterials 32(29):7060–7067.  https://doi.org/10.1016/j.biomaterials.2011.06.008 CrossRefPubMedGoogle Scholar
  49. 49.
    Gothard D, Smith EL, Kanczler JM, Black CR, Wells JA, Roberts CA, White LJ, Qutachi O, Peto H, Rashidi H, Rojo L, Stevens MM, El Haj AJ, Rose FR, Shakesheff KM, Oreffo RO (2015) In vivo assessment of bone regeneration in alginate/bone ECM hydrogels with incorporated skeletal stem cells and single growth factors. PLoS One 10(12):e0145080.  https://doi.org/10.1371/journal.pone.0145080 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Marolt D, Campos IM, Bhumiratana S, Koren A, Petridis P, Zhang G, Spitalnik PF, Grayson WL, Vunjak-Novakovic G (2012) Engineering bone tissue from human embryonic stem cells. Proc Natl Acad Sci U S A 109(22):8705–8709.  https://doi.org/10.1073/pnas.1201830109 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Grayson WL, Marolt D, Bhumiratana S, Frohlich M, Guo XE, Vunjak-Novakovic G (2011) Optimizing the medium perfusion rate in bone tissue engineering bioreactors. Biotechnol Bioeng 108(5):1159–1170.  https://doi.org/10.1002/bit.23024 CrossRefPubMedGoogle Scholar
  52. 52.
    Temenoff JS, Mikos AG (2000) Review: tissue engineering for regeneration of articular cartilage. Biomaterials 21(5):431–440CrossRefGoogle Scholar
  53. 53.
    Kock L, van Donkelaar CC, Ito K (2012) Tissue engineering of functional articular cartilage: the current status. Cell Tissue Res 347(3):613–627.  https://doi.org/10.1007/s00441-011-1243-1 CrossRefPubMedGoogle Scholar
  54. 54.
    Sophia Fox AJ, Bedi A, Rodeo SA (2009) The basic science of articular cartilage: structure, composition, and function. Sports Health 1(6):461–468.  https://doi.org/10.1177/1941738109350438 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Makris EA, Gomoll AH, Malizos KN, Hu JC, Athanasiou KA (2015) Repair and tissue engineering techniques for articular cartilage. Nat Rev Rheumatol 11(1):21–34.  https://doi.org/10.1038/nrrheum.2014.157 CrossRefPubMedGoogle Scholar
  56. 56.
    Ahn CB, Kim Y, Park SJ, Hwang Y, Lee JW (2017) Development of arginine-glycine-aspartate-immobilized 3D printed poly(propylene fumarate) scaffolds for cartilage tissue engineering. J Biomater Sci Polym Ed 1–15.  https://doi.org/10.1080/09205063.2017.1383020 CrossRefGoogle Scholar
  57. 57.
    Benders KE, van Weeren PR, Badylak SF, Saris DB, Dhert WJ, Malda J (2013) Extracellular matrix scaffolds for cartilage and bone regeneration. Trends Biotechnol 31(3):169–176.  https://doi.org/10.1016/j.tibtech.2012.12.004 CrossRefPubMedGoogle Scholar
  58. 58.
    Burdick JA, Mauck RL, Gorman JH 3rd, Gorman RC (2013) Acellular biomaterials: an evolving alternative to cell-based therapies. Sci Transl Med 5(176):176ps4.  https://doi.org/10.1126/scitranslmed.3003997 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Gong YY, Xue JX, Zhang WJ, Zhou GD, Liu W, Cao Y (2011) A sandwich model for engineering cartilage with acellular cartilage sheets and chondrocytes. Biomaterials 32(9):2265–2273.  https://doi.org/10.1016/j.biomaterials.2010.11.078 CrossRefPubMedGoogle Scholar
  60. 60.
    Rowland CR, Colucci LA, Guilak F (2016) Fabrication of anatomically-shaped cartilage constructs using decellularized cartilage-derived matrix scaffolds. Biomaterials 91:57–72.  https://doi.org/10.1016/j.biomaterials.2016.03.012 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Yang Q, Peng J, Guo Q, Huang J, Zhang L, Yao J, Yang F, Wang S, Xu W, Wang A, Lu S (2008) A cartilage ECM-derived 3-D porous acellular matrix scaffold for in vivo cartilage tissue engineering with PKH26-labeled chondrogenic bone marrow-derived mesenchymal stem cells. Biomaterials 29(15):2378–2387.  https://doi.org/10.1016/j.biomaterials.2008.01.037 CrossRefPubMedGoogle Scholar
  62. 62.
    Kang H, Peng J, Lu S, Liu S, Zhang L, Huang J, Sui X, Zhao B, Wang A, Xu W, Luo Z, Guo Q (2014) In vivo cartilage repair using adipose-derived stem cell-loaded decellularized cartilage ECM scaffolds. J Tissue Eng Regen Med 8(6):442–453.  https://doi.org/10.1002/term.1538 CrossRefPubMedGoogle Scholar
  63. 63.
    Sutherland AJ, Beck EC, Dennis SC, Converse GL, Hopkins RA, Berkland CJ, Detamore MS (2015) Decellularized cartilage may be a chondroinductive material for osteochondral tissue engineering. PLoS One 10(5):e0121966.  https://doi.org/10.1371/journal.pone.0121966 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Yin H, Wang Y, Sun Z, Sun X, Xu Y, Li P, Meng H, Yu X, Xiao B, Fan T, Wang Y, Xu W, Wang A, Guo Q, Peng J, Lu S (2016) Induction of mesenchymal stem cell chondrogenic differentiation and functional cartilage microtissue formation for in vivo cartilage regeneration by cartilage extracellular matrix-derived particles. Acta Biomater 33:96–109.  https://doi.org/10.1016/j.actbio.2016.01.024 CrossRefPubMedGoogle Scholar
  65. 65.
    Pati F, Jang J, Ha DH, Won Kim S, Rhie JW, Shim JH, Kim DH, Cho DW (2014) Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat Commun 5:3935.  https://doi.org/10.1038/ncomms4935 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Teodori L, Costa A, Marzio R, Perniconi B, Coletti D, Adamo S, Gupta B, Tarnok A (2014) Native extracellular matrix: a new scaffolding platform for repair of damaged muscle. Front Physiol 5:218.  https://doi.org/10.3389/fphys.2014.00218 CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Qazi TH, Mooney DJ, Pumberger M, Geissler S, Duda GN (2015) Biomaterials based strategies for skeletal muscle tissue engineering: existing technologies and future trends. Biomaterials 53:502–521.  https://doi.org/10.1016/j.biomaterials.2015.02.110 CrossRefGoogle Scholar
  68. 68.
    Crawley S, Farrell EM, Wang W, Gu M, Huang HY, Huynh V, Hodges BL, Cooper DN, Kaufman SJ (1997) The alpha7beta1 integrin mediates adhesion and migration of skeletal myoblasts on laminin. Exp Cell Res 235(1):274–286.  https://doi.org/10.1006/excr.1997.3671 CrossRefPubMedGoogle Scholar
  69. 69.
    Gillies AR, Lieber RL (2011) Structure and function of the skeletal muscle extracellular matrix. Muscle Nerve 44(3):318–331.  https://doi.org/10.1002/mus.22094 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Wang YX, Rudnicki MA (2011) Satellite cells, the engines of muscle repair. Nat Rev Mol Cell Biol 13(2):127–133.  https://doi.org/10.1038/nrm3265 CrossRefPubMedGoogle Scholar
  71. 71.
    Hwang Y, Seo T, Hariri S, Choi C, Varghese S (2017) Matrix topographical cue-mediated myogenic differentiation of human embryonic stem cell derivatives. Polymers 9(11):580CrossRefGoogle Scholar
  72. 72.
    Conconi MT, De Coppi P, Bellini S, Zara G, Sabatti M, Marzaro M, Zanon GF, Gamba PG, Parnigotto PP, Nussdorfer GG (2005) Homologous muscle acellular matrix seeded with autologous myoblasts as a tissue-engineering approach to abdominal wall-defect repair. Biomaterials 26(15):2567–2574.  https://doi.org/10.1016/j.biomaterials.2004.07.035 CrossRefPubMedGoogle Scholar
  73. 73.
    Merritt EK, Hammers DW, Tierney M, Suggs LJ, Walters TJ, Farrar RP (2010) Functional assessment of skeletal muscle regeneration utilizing homologous extracellular matrix as scaffolding. Tissue Eng Part A 16(4):1395–1405.  https://doi.org/10.1089/ten.TEA.2009.0226 CrossRefPubMedGoogle Scholar
  74. 74.
    DeQuach JA, Lin JE, Cam C, Hu D, Salvatore MA, Sheikh F, Christman KL (2012) Injectable skeletal muscle matrix hydrogel promotes neovascularization and muscle cell infiltration in a hindlimb ischemia model. Eur Cell Mater 23:400–412 discussion 12CrossRefGoogle Scholar
  75. 75.
    Ungerleider JL, Johnson TD, Rao N, Christman KL (2015) Fabrication and characterization of injectable hydrogels derived from decellularized skeletal and cardiac muscle. Methods 84:53–59.  https://doi.org/10.1016/j.ymeth.2015.03.024 CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Stern MM, Myers RL, Hammam N, Stern KA, Eberli D, Kritchevsky SB, Soker S, Van Dyke M (2009) The influence of extracellular matrix derived from skeletal muscle tissue on the proliferation and differentiation of myogenic progenitor cells ex vivo. Biomaterials 30(12):2393–2399.  https://doi.org/10.1016/j.biomaterials.2008.12.069 CrossRefPubMedGoogle Scholar
  77. 77.
    DeQuach JA, Mezzano V, Miglani A, Lange S, Keller GM, Sheikh F, Christman KL (2010) Simple and high yielding method for preparing tissue specific extracellular matrix coatings for cell culture. PLoS One 5(9):e13039.  https://doi.org/10.1371/journal.pone.0013039 CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Chaturvedi V, Dye DE, Kinnear BF, van Kuppevelt TH, Grounds MD, Coombe DR (2015) Interactions between skeletal muscle myoblasts and their extracellular matrix revealed by a serum free culture system. PLoS One 10(6):e0127675.  https://doi.org/10.1371/journal.pone.0127675 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Merritt EK, Cannon MV, Hammers DW, Le LN, Gokhale R, Sarathy A, Song TJ, Tierney MT, Suggs LJ, Walters TJ, Farrar RP (2010) Repair of traumatic skeletal muscle injury with bone-marrow-derived mesenchymal stem cells seeded on extracellular matrix. Tissue Eng Part A 16(9):2871–2881.  https://doi.org/10.1089/ten.TEA.2009.0826 CrossRefPubMedGoogle Scholar
  80. 80.
    Rao N, Agmon G, Tierney MT, Ungerleider JL, Braden RL, Sacco A, Christman KL (2017) Engineering an injectable muscle-specific microenvironment for improved cell delivery using a nanofibrous extracellular matrix hydrogel. ACS Nano 11(4):3851–3859.  https://doi.org/10.1021/acsnano.7b00093 CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Choi YJ, Kim TG, Jeong J, Yi HG, Park JW, Hwang W, Cho DW (2016) 3D cell printing of functional skeletal muscle constructs using skeletal muscle-derived bioink. Adv Healthc Mater 5(20):2636–2645.  https://doi.org/10.1002/adhm.201600483 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Hyunbum Kim
    • 1
    • 2
  • Yunhye Kim
    • 2
  • Mona Fendereski
    • 2
  • Nathaniel S. Hwang
    • 1
  • Yongsung Hwang
    • 2
    Email author
  1. 1.School of Chemical and Biological EngineeringInstitute of Chemical Processes, Seoul National UniversitySeoulSouth Korea
  2. 2.Soonchunhyang Institute of Medi-bio Science (SIMS)Soonchunhyang UniversityCheonan-siSouth Korea

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