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Angiogenic potential of extracellular matrix of human amniotic membrane

Tissue Engineering and Regenerative Medicine volume 13, pages 211–217 (2016)Cite this article

Abstract

Combination between tissue engineering and other fields has brought an innovation in the area of regenerative medicine which ultimate aims are to repair, improve, and produce a good tissue construct. The availability of many types of scaffold, both synthetically and naturally have developed into many outstanding end products that have achieved the general objective in tissue engineering. Interestingly, most of this scaffold emulates extracellular matrix (ECM) characteristics. Therefore, ECM component sparks an interest to be explored and manipulated. The ECM featured in human amniotic membrane (HAM) provides a suitable niche for the cells to adhere, grow, proliferate, migrate and differentiate, and could possibly contribute to the production of angiogenic micro-environment indirectly. Previously, HAM scaffold has been widely used to accelerate wound healing, treat bone related and ocular diseases, and involved in cardiovascular repair. Also, it has been used in the angiogenicity study, but with a different technical approach. In addition, both side of HAM could be used in cellularised and decellularised conditions depending on the objectives of a particular research. Therefore, it is of paramount importance to investigate the behavior of ECM components especially on the stromal side of HAM and further explore the angiogenic potential exhibited by this scaffold.

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References

  1. Dhandayuthapani B, Yoshida Y, Maekawa T, Kumar DS. Polymeric scaffolds in tissue engineering application: a review. Int J Polym Sci 2011 [Epub]. DOI:10.1155/2011/290602.

    Google Scholar 

  2. Toda A, Okabe M, Yoshida T, Nikaido T. The potential of amniotic membrane/amnion-derived cells for regeneration of various tissues. J Pharmacol Sci 2007;105:215–228.

    Article  CAS  PubMed  Google Scholar 

  3. Barbara Z, Eriberto B, Stefano S, Giulia B, Chiara G, Ferrarese N, et al. Dental Pulp Stem Cells and Tissue Engineering Strategies for Clinical Application on Odontoiatric Field. In: Pignatello R, editor. Biomaterials Science and Engineering. Croatia: InTech; 2011. p.339–348.

    Google Scholar 

  4. Nakashima M, Iohara K, Sugiyama M. Human dental pulp stem cells with highly angiogenic and neurogenic potential for possible use in pulp regeneration. Cytokine Growth Factor Rev 2009;20:435–440.

    Article  CAS  PubMed  Google Scholar 

  5. Zisch AH, Lutolf MP, Hubbell JA. Biopolymeric delivery matrices for angiogenic growth factors. Cardiovasc Pathol 2003;12:295–310.

    Article  CAS  PubMed  Google Scholar 

  6. Niknejad H, Peirovi H, Jorjani M, Ahmadiani A, Ghanavi J, Seifalian AM. Properties of the amniotic membrane for potential use in tissue engi neering. Eur Cell Mater 2008;15:88–99.

    CAS  PubMed  Google Scholar 

  7. Murray PE, Garcia-Godoy F, Hargreaves KM. Regenerative endodontics: a review of current status and a call for action. J Endod 2007;33:377–390.

    Article  PubMed  Google Scholar 

  8. Kanczler JM, Oreffo RO. Osteogenesis and angiogenesis: the potential for engineering bone. Eur Cell Mater 2008;15:100–114.

    CAS  PubMed  Google Scholar 

  9. Huang GT, Sonoyama W, Chen J, Park SH. In vitro characterization of human dental pulp cells: various isolation methods and culturing environments. Cell Tissue Res 2006;324:225–236.

    Article  PubMed  Google Scholar 

  10. Plant AL, Bhadriraju K, Spurlin TA, Elliott JT. Cell response to matrix mechanics: focus on collagen. Biochim Biophys Acta 2009;1793:893–902.

    Article  CAS  PubMed  Google Scholar 

  11. Sieminski AL, Gooch KJ. Biomaterial-microvasculature interactions. Biomaterials 2000;21:2232–2241.

    Article  CAS  PubMed  Google Scholar 

  12. Heil M, Eitenmüller I, Schmitz-Rixen T, Schaper W. Arteriogenesis versus angiogenesis: similarities and differences. J Cell Mol Med 2006; 10:45–55.

    Article  CAS  PubMed  Google Scholar 

  13. Carmeliet P. Angiogenesis in health and disease. Nat Med 2003;9:653–660.

    Article  CAS  PubMed  Google Scholar 

  14. Djonov V, Makanya AN. New insights into intussusceptive angiogenesis. EXS 2005;(94):17–33.

    PubMed  Google Scholar 

  15. Cordeiro MM, Dong Z, Kaneko T, Zhang Z, Miyazawa M, Shi S, et al. Dental pulp tissue engineering with stem cells from exfoliated deciduous teeth. J Endod 2008;34:962–969.

    Article  PubMed  Google Scholar 

  16. Demarco FF, Conde MC, Cavalcanti BN, Casagrande L, Sakai VT, Nör JE. Dental pulp tissue engineering. Braz Dent J 2011;22:3–13.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Jabbarzadeh E, Starnes T, Khan YM, Jiang T, Wirtel AJ, Deng M, et al. Induction of angiogenesis in tissue-engineered scaffolds designed for bone repair: a combined gene therapy-cell transplantation approach. Proc Natl Acad Sci U S A 2008;105:11099–11104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Arkudas A, Balzer A, Buehrer G, Arnold I, Hoppe A, Detsch R, et al. Evaluation of angiogenesis of bioactive glass in the arteriovenous loop model. Tissue Eng Part C Methods 2013;19:479–486.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Leach JK, Kaigler D, Wang Z, Krebsbach PH, Mooney DJ. Coating of VEGF-releasing scaffolds with bioactive glass for angiogenesis and bone regeneration. Biomaterials 2006;27:3249–3255.

    Article  CAS  PubMed  Google Scholar 

  20. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature 2000;407:249–257.

    Article  CAS  PubMed  Google Scholar 

  21. Sun J, Wang Y, Qian Z, Hu C. An approach to architecture 3D scaffold with interconnective microchannel networks inducing angiogenesis for tissue engineering. J Mater Sci Mater Med 2011;22:2565–2571.

    Article  CAS  PubMed  Google Scholar 

  22. Li Z, Qu T, Ding C, Ma C, Sun H, Li S, et al. Injectable gelatin derivative hydrogels with sustained vascular endothelial growth factor release for induced angiogenesis. Acta Biomater 2015;13:88–100.

    Article  CAS  PubMed  Google Scholar 

  23. Mittermayr R, Morton T, Hofmann M, Helgerson S, van Griensven M, Redl H. Sustained (rh)VEGF(165) release from a sprayed fibrin biomatrix induces angiogenesis, up-regulation of endogenous VEGF-R2, and reduces ischemic flap necrosis. Wound Repair Regen 2008;16:542–550.

    Article  PubMed  Google Scholar 

  24. Moon JJ, West JL. Vascularization of engineered tissues: approaches to promote angio-genesis in biomaterials. Curr Top Med Chem 2008;8: 300–310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Brennan JA, Arrizabalaga JH, Nollert MU. Development of a small diameter vascular graft using the human amniotic membrane. Cardiovasc Eng Techno 2014;5:96–109.

    Article  Google Scholar 

  26. Caruso M, Silini A, Parolini O. The human amniotic membrane: A tissue with multifaceted properties and different potential clinical applications. In: Kyle JC, Curtis L, Cetrulo Jr, Rouzbeh R, Taghizadeh A, editors. Perinatal Stem Cells. 2nd ed. New Jersey: John Wiley & Sons; 2013. p.177–195.

    Chapter  Google Scholar 

  27. Chopra A, Thomas BS. Amniotic membrane: a novel material for regeneration and repair. J Biomim Biomater Tissue Eng 2013;18:106.

    Google Scholar 

  28. Riau AK, Beuerman RW, Lim LS, Mehta JS. Preservation, sterilization and de-epithelialization of human amniotic membrane for use in ocular surface reconstruction. Biomaterials 2010;31:216–225.

    Article  CAS  PubMed  Google Scholar 

  29. Koizumi NJ, Inatomi TJ, Sotozono CJ, Fullwood NJ, Quantock AJ, Kinoshita S. Growth factor mRNA and protein in preserved human amniotic membrane. Curr Eye Res 2000;20:173–177.

    Article  CAS  PubMed  Google Scholar 

  30. Nor Kamalia Z, Suzina SAH, Yusof N. Changes in biophysical properties of human amniotic membranes after different preservation methods and radiation sterilization. Regen Res 2014;3:64–70.

    Google Scholar 

  31. Ab Hamid SS, Zahari NK, Yusof N, Hassan A. Scanning electron microscopic assessment on surface morphology of preserved human amniotic membrane after gamma sterilisation. Cell Tissue Bank 2014;15:15–24.

    Article  PubMed  Google Scholar 

  32. Taghiabadi E, Nasri S, Shafieyan S, Jalili Firoozinezhad S, Aghdami N. Fabrication and characterization of spongy denuded amniotic membrane based scaffold for tissue engineering. Cell J 2015;16:476–487.

    PubMed  PubMed Central  Google Scholar 

  33. Madri JA, Williams SK. Capillary endothelial cell cultures: phenotypic modulation by matrix components. J Cell Biol 1983;97:153–165.

    Article  CAS  PubMed  Google Scholar 

  34. Wolbank S, Hildner F, Redl H, van Griensven M, Gabriel C, Hennerbichler S. Impact of human amniotic membrane preparation on release of angiogenic factors. J Tissue Eng Regen Med 2009;3:651–654.

    Article  CAS  PubMed  Google Scholar 

  35. Ma DH, Yao JY, Yeh LK, Liang ST, See LC, Chen HT, et al. In vitro antiangiogenic activity in ex vivo expanded human limbocorneal epithelial cells cultivated on human amniotic membrane. Invest Ophthalmol Vis Sci 2004;45:2586–2595.

    Article  PubMed  Google Scholar 

  36. Tsai SH, Liu YW, Tang WC, Zhou ZW, Hwang CY, Hwang GY, et al. Characterization of porcine arterial endothelial cells cultured on amniotic membrane, a potential matrix for vascular tissue engineering. Biochem Biophys Res Commun 2007;357:984–990.

    Article  CAS  PubMed  Google Scholar 

  37. Maral T, Borman H, Arslan H, Demirhan B, Akinbingol G, Haberal M. Effectiveness of human amnion preserved long-term in glycerol as a temporary biological dressing. Burns 1999;25:625–635.

    Article  CAS  PubMed  Google Scholar 

  38. Bose B. Burn wound dressing with human amniotic membrane. Ann R Coll Surg Engl 1979;61:444–447.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Yang L, Shirakata Y, Tokumaru S, Xiuju D, Tohyama M, Hanakawa Y, et al. Living skin equivalents constructed using human amnions as a matrix. J Dermatol Sci 2009;56:188–195.

    Article  CAS  PubMed  Google Scholar 

  40. Starecki M, Razzano P, Schwartz JA, Grande DA. Evaluation of amniotic derived membrane biomaterial as an adjunct for repair of critical sized bone defects. Adv Orthop Surg 2014 ID 572586.

    Google Scholar 

  41. Díaz-Prado S, Rendal-Vázquez ME, Muiños-López E, Hermida-Gómez T, Rodríguez-Cabarcos M, Fuentes-Boquete I, et al. Potential use of the human amniotic membrane as a scaffold in human articular cartilage repair. Cell Tissue Bank 2010;11:183–195.

    Article  PubMed  Google Scholar 

  42. Jin CZ, Park SR, Choi BH, Lee KY, Kang CK, Min BH. Human amniotic membrane as a delivery matrix for articular cartilage repair. Tissue Eng 2007;13:693–702.

    Article  CAS  PubMed  Google Scholar 

  43. Grueterich M, Espana EM, Tseng SC. Ex vivo expansion of limbal epithelial stem cells: amniotic membrane serving as a stem cell niche. Surv Ophthalmol 2003;48:631–646.

    Article  PubMed  Google Scholar 

  44. Solomon A, Rosenblatt M, Monroy D, Ji Z, Pflugfelder SC, Tseng SC. Suppression of interleukin 1alpha and interleukin 1beta in human limbal epithelial cells cultured on the amniotic membrane stromal matrix. Br J Ophthalmol 2001;85:444–449.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ishino Y, Sano Y, Nakamura T, Connon CJ, Rigby H, Fullwood NJ, et al. Amniotic membrane as a carrier for cultivated human corneal endothelial cell transplantation. Invest Ophthalmol Vis Sci 2004;45:800–806.

    Article  PubMed  Google Scholar 

  46. Lo V, Pope E. Amniotic membrane use in dermatology. Int J Dermatol 2009;48:935–940.

    Article  CAS  PubMed  Google Scholar 

  47. Hopkinson A, Shanmuganathan VA, Gray T, Yeung AM, Lowe J, James DK, et al. Optimization of amniotic membrane (AM) denuding for tissue engineering. Tissue Eng Part C Methods 2008;14:371–381.

    Article  CAS  PubMed  Google Scholar 

  48. Liu J, Sheha H, Fu Y, Liang L, Tseng SC. Update on amniotic membrane transplantation. Expert Rev Ophthalmol 2010;5:645–661.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Burgos H. Angiogenic factor from human term placenta. Purification and partial characterization. Eur J Clin Invest 1986;16:486–493.

    Article  CAS  PubMed  Google Scholar 

  50. Langer R, Tirrell DA. Designing materials for biology and medicine. Nature 2004;428:487–492.

    Article  CAS  PubMed  Google Scholar 

  51. Geiger B, Bershadsky A, Pankov R, Yamada KM. Transmembrane cross talk between the extracellular matrix—cytoskeleton crosstalk. Nat Rev Mol Cell Biol 2001;2:793–805.

    Article  CAS  PubMed  Google Scholar 

  52. Bowers SL, Banerjee I, Baudino TA. The extracellular matrix: at the center of it all. J Mol Cell Cardiol 2010;48:474–482.

    Article  CAS  PubMed  Google Scholar 

  53. Cukierman E, Pankov R, Yamada KM. Cell interactions with three-dimensional matrices. Curr Opin Cell Biol 2002;14:633–639.

    Article  CAS  PubMed  Google Scholar 

  54. Bayless KJ, Salazar R, Davis GE. RGD-dependent vacuolation and lumen formation observed during endothelial cell morphogenesis in threedimensional fibrin matrices involves the alpha(v)beta(3) and alpha(5) beta(1) integrins. Am J Pathol 2000;156:1673–1683.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Miyamoto S, Teramoto H, Gutkind JS, Yamada KM. Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activation: roles of integrin aggregation and occupancy of receptors. J Cell Biol 1996;135(6 Pt 1):1633–1642.

    Article  CAS  PubMed  Google Scholar 

  56. Astrof S, Hynes RO. Fibronectins in vascular morphogenesis. Angiogenesis 2009;12:165–175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Zhang YQ, Ji SZ, Fang H, Zheng YJ, Luo PF, Wu HB, et al. Use of amniotic microparticles coated with fibroblasts overexpressing SDF-1a to create an environment conducive to neovascularization for repair of fullthickness skin defects. Cell Transplant 2015;25:365–376.

    Article  PubMed  Google Scholar 

  58. Brauer R, Beck IM, Roderfeld M, Roeb E, Sedlacek R. Matrix metalloproteinase-19 inhibits growth of endothelial cells by generating angiostatin-like fragments from plasminogen. BMC Biochem 2011;12:38.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Mavria G, Vercoulen Y, Yeo M, Paterson H, Karasarides M, Marais R, et al. ERK-MAPK signaling opposes Rho-kinase to promote endothelial cell survival and sprouting during angiogenesis. Cancer Cell 2006;9:33–44.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. School of Dental Sciences, Universiti Sains Malaysia, Health Campus, 16150, Kelantan, Malaysia

    Siti Nurnasihah Md Hashim, Muhammad Fuad Hilmi Yusof, Wafa’ Zahari, Khairul Bariah Ahmad Amin Noordin, Thirumulu Ponnuraj Kannan & Azlina Ahmad

  2. Human Genome Centre, School of Medical Sciences, Universiti Sains Malaysia, Kelantan, Malaysia

    Thirumulu Ponnuraj Kannan

  3. Tissue Bank, School of Medical Sciences, Universiti Sains Malaysia, Kelantan, Malaysia

    Suzina Sheikh Abdul Hamid

  4. Kulliyyah of Dentistry, International Islamic University Malaysia, Pahang, Malaysia

    Khairani Idah Mokhtar

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  1. Siti Nurnasihah Md Hashim
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  2. Muhammad Fuad Hilmi Yusof
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  3. Wafa’ Zahari
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  8. Azlina Ahmad
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Correspondence to Azlina Ahmad.

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Hashim, S.N.M., Yusof, M.F.H., Zahari, W. et al. Angiogenic potential of extracellular matrix of human amniotic membrane. Tissue Eng Regen Med 13, 211–217 (2016). https://doi.org/10.1007/s13770-016-9057-6

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  • DOI: https://doi.org/10.1007/s13770-016-9057-6

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