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Cytotechnology

, Volume 58, Issue 1, pp 49–56 | Cite as

Alginate cell encapsulation: new advances in reproduction and cartilage regenerative medicine

  • Ilaria Ghidoni
  • Theodora Chlapanidas
  • Massimo Bucco
  • Francesca Crovato
  • Mario Marazzi
  • Daniele Vigo
  • Maria Luisa Torre
  • Massimo FaustiniEmail author
Special Issue Stem Cells

Abstract

Cell encapsulation, a strategy whereby a pool of live cells is entrapped within a semipermeable membrane, represents an evolving branch of biotechnology and regenerative medicine. For example, over the last 20 years, male and female gametes and embryos have been encapsulated with or without somatic cells for different purposes, such as in vitro gametogenesis, embryo culture, cell preservation and semen controlled release. Beside that, cell encapsulation technology in alginate, which is a natural biodegradable polymer that mimics the extracellular matrix and supports both cell functions and metabolism, has been developed with the aim of obtaining three-dimensional (3D) cultures. In this context, adipose-derived stromal vascular fraction (SVF) has attracted more and more attention because of its enormous potential in tissue regeneration. In fact, the SVF represents a rich source of mesenchymal cells (ADSCs), potentially able to differentiate into adipocytes, chondrocytes, osteoblasts, myocytes, cardiomyocytes, hepatocytes, and neuronal, epithelial and endothelial cells. These cells are ideal candidates for use in regenerative medicine, tissue engineering, including gene therapy and cell replacement cancer therapies. As long as technological resources are available for large-scale cell encapsulation intended for advanced therapies (gene therapy, somatic cell therapy and tissue engineering), the state-of-the-art in this field is reviewed in terms of scientific literature.

Keywords

Alginate Cell encapsulation Gametes Intervertebral disc regenerative therapy Adipose-derived stem cells 

References

  1. Andrè P (2002) Facial lipoatrophy secondary to a new synthetic filler device (Profill) treated by lipofilling. J Cosmet Dermatol 1:59–61. doi: 10.1046/j.1473-2165.2002.00044.x CrossRefGoogle Scholar
  2. Barrilleux B, Phinney DG, Prockop DJ, O’Connor K (2006) Review: ex-vivo engineering of living tissues with adult stem cells. Tissue Eng 12:3007–3019. doi: 10.1089/ten.2006.12.3007 CrossRefGoogle Scholar
  3. Benzoni E, Torre ML, Faustini M, Stacchezzini S, Cremonesi F, Conte U, Villani S, Russo V, Ricevuti G, Vigo D (2005) Transient transfection of porcine granulosa cells after 3D culture in barium alginate capsules. Int J Immunopathol Pharmacol 18:677–682Google Scholar
  4. Bissell MJ, Rizki A, Mian IS (2003) Tissue architecture: the ultimate regulator of breast epithelial function. Curr Opin Cell Biol 15:753–762. doi: 10.1016/j.ceb.2003.10.016 CrossRefGoogle Scholar
  5. Braccini I, Pérez S (2001) Molecular basis of C(2+)-induced gelation in alginates and pectins: the egg-box model revisited. Biomacromolecules 2:1089–1096. doi: 10.1021/bm010008g CrossRefGoogle Scholar
  6. Brzoska M, Geiger H, Gauer S, Baer P (2005) Epithelial differentiation of human adipose tissue-derived adult stem cells. Biochem Biophys Res Commun 330:142–150. doi: 10.1016/j.bbrc.2005.02.141 CrossRefGoogle Scholar
  7. Casteilla L, Charrière G, Laharrague P, Cousin B, Planat-Benard V, Pèricaud L, Chavoin JP (2004) Adipose tissue, plastic and reconstructive surgery: come back to sources. Ann Chir Plast Esthet 49:409–418. doi: 10.1016/j.anplas.2004.08.001 CrossRefGoogle Scholar
  8. Chang TMS (1964) Semipermeable microcapslules. Science 146:524–525. doi: 10.1126/science.146.3643.524 CrossRefGoogle Scholar
  9. Coleman SR (2004) Rèinjection de graisse autologue ou lipofilling ou Lipostructure®. Ann Chir Plast Esthet 49:456–458. doi: 10.1016/j.anplas.2004.09.005 CrossRefGoogle Scholar
  10. Conte U, Torre ML, Maggi L, Giunchedi P, Vigo D, Maffeo G, Russo V (1999) EP0922451Google Scholar
  11. De Ugarte DA, Ashjian PH, Elbarbary A, Hedrick MH (2003) Future of fat as raw material for tissue regeneration. Ann Plast Surg 50:215–219. doi: 10.1097/01.SAP.0000029661.38066.15 CrossRefGoogle Scholar
  12. Dicker A, LeBlanc K, Åstrom G, van Harmelen V, Götherström C, Blomqvist L, Arner P, Rydén M (2005) Functional studies of mesenchymal stem cells derived from adult human adipose tissue. Exp Cell Res 308:283–290. doi: 10.1016/j.yexcr.2005.04.029 CrossRefGoogle Scholar
  13. Draget KI, Gaserod O, Aune I (2001) Effects of molecular weight and elastic segment flexibility on syneresis in Ca alginate gels. Food Hydrocoll 15:485–490. doi: 10.1016/S0268-005X(01)00046-7 CrossRefGoogle Scholar
  14. Ellenborgen R (2000) Fat transfer: current use in practise. Cinical Plast Surg 27:545–546Google Scholar
  15. Even-Ram S, Yamada KM (2005) Cell migration in 3D matrix. Curr Opin Cell Biol 17:524–532. doi: 10.1016/j.ceb.2005.08.015 CrossRefGoogle Scholar
  16. Fraser JK, Wulur I, Alfonso Z, Hedrick MH (2006) Fat tissue an underappreciated source of stem cells for biotechnology. Trends Biotechnol 24:150–154. doi: 10.1016/j.tibtech.2006.01.010 CrossRefGoogle Scholar
  17. Gaetani P, Torre ML, Klinger M, Faustini M, Crovato F, Bucco M, Marazzi M, Chlapanidas T, Levi D, Tancioni F, Vigo D, Rodriguez y Baena R (2008) Adipose-derived stem cell therapy for intervertebral disc regeneration: an in vitro reconstructed tissue in alginate capsules. Tissue Eng Part A 141:415–423Google Scholar
  18. Gomillion CT, Burg K (2006) Stem cells and adipose tissue engineering. Biomaterials 27:6052–6605. doi: 10.1016/j.biomaterials.2006.07.033 CrossRefGoogle Scholar
  19. Goosen MF, O’Shea GM, Gharapetian HM, Chou S, Sun AM (1985) Optimization of microencapsulation parameters: Semipermeable microcapsules as a bioartificial pancreas. Biotechnol Bioeng 27(2):146–150. doi: 10.1002/bit.260270207 CrossRefGoogle Scholar
  20. Griffith LG, Naughton G (2002) Tissue engineering—current challenges and expanding opportunities. Science 295:1009–1014. doi: 10.1126/science.1069210 CrossRefGoogle Scholar
  21. Guilak F, Lott KE, Awad HA, Cao Q, Hicok KC, Fermor B, Gimble JM (2006) Clonal analysis of the differentiation potential of human adipose-derived adult stem cells. J Cell Physiol 206:229–237. doi: 10.1002/jcp.20463 CrossRefGoogle Scholar
  22. Helder MN, Knippenberg M, Klein-Nulend J, Wuisman PI (2007) Stem cells from adipose tissue allow challenging new concepts for regenerative medicine. Tissue Eng 13:1799–1808. doi: 10.1089/ten.2006.0165 CrossRefGoogle Scholar
  23. Herrler A, Eisner S, Bach V, Weissenborn U, Beier HM (2006) Cryopreservation of spermatozoa in alginic acid capsules. Fertil Steril 85:208–213. doi: 10.1016/j.fertnstert.2005.06.049 CrossRefGoogle Scholar
  24. Johnson LA, Weitze KF, Fiser P, Mawxell WMC (2000) Storage of boar semen. Anim Reprod Sci 62:143–172. doi: 10.1016/S0378-4320(00)00157-3 CrossRefGoogle Scholar
  25. Klinger M, Marazzi M, Vigo D, Torre ML (2008) Fat injection in severe burn outcomes: a new perspective of scar remodelling and reduction. Aesthetic Plast Surg 32:465–469. doi: 10.1007/s00266-008-9122-1 CrossRefGoogle Scholar
  26. Lee J, Cuddihy MJ, Kotov NA (2008) Three-dimensional cell culture matrices: state of the art. Tissue Eng Part B 1:61–86. doi: 10.1089/teb.2007.0150 CrossRefGoogle Scholar
  27. Li X, Lee JP, Balian G, Anderson DG (2005) Modulation of chondrocytic properties of fat-derived mesenchymal cells in co-cultures with nucleus pulposus. Connect Tissue Res 46:75–82. doi: 10.1080/03008200590954104 CrossRefGoogle Scholar
  28. Lim F, Sun AM (1980) Microencapsulated islets as bioartificial endocrine pancreas. Science 210:908–910. doi: 10.1126/science.6776628 CrossRefGoogle Scholar
  29. Liu WF, Chen CS (2007) Cellular and multicellular form and function. Adv Drug Deliv Rev 59:1319–1328. doi: 10.1016/j.addr.2007.08.011 CrossRefGoogle Scholar
  30. Lukashev ME, Werb Z (1998) ECM signalling: orchestrating cell behaviour and misbehaviour. Trends Cell Biol 8:437–441. doi: 10.1016/S0962-8924(98)01362-2 CrossRefGoogle Scholar
  31. Martina M, Hutmacher DW (2007) Biodegradable polymers applied in tissue engineering research: a review. Polym Int 56:145–151. doi: 10.1002/pi.2108 CrossRefGoogle Scholar
  32. Matsumoto D, Sato K, Gonda K, Takaki Y, Shigeura T, Sato T, Aiba-Kojima E, Iizura F, Keita I, Suga H, Yoshimura K (2006) Cell-assisted lipotransfer: supportive use of human adipose-derived cells for soft tissue augmentation with lipoinjection. Tissue Eng 12:3375–3381. doi: 10.1089/ten.2006.12.3375 CrossRefGoogle Scholar
  33. Maxwell WMC, Johnson LA (1999) Physiology of spermatozoa at high dilution rates: the influence of seminal plasma. Theriogenology 52:1353–1362. doi: 10.1016/S0093-691X(99)00222-8 CrossRefGoogle Scholar
  34. Mitchell JB, McIntosh K, Zvonic S, Garrett S, Floyd ZE, Kloster A, Di Halvorsen Y, Storms RW, Goh B, Kilroy G, Wu X, Gimble JM (2006) Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem Cells 24:376–385. doi: 10.1634/stemcells.2005-0234 CrossRefGoogle Scholar
  35. Mizuno H, Hyakusoku H (2003) Mesengenic potential and future clinical perspective of human processed lipoaspirate cells. J Nippon Med Sch 70:300–306. doi: 10.1272/jnms.70.300 CrossRefGoogle Scholar
  36. Munkittrick TW, Nebel RL, Saacke RG (1992) Accessory sperm numbers for cattle inseminated with protamine sulphate microcapsules. J Dairy Sci 75:725–731CrossRefGoogle Scholar
  37. Munoz-Garay C, De la Vega-Beltràn JL, Delgado R (2001) Inwardly rectify K+ channels in spermatogenic cells: functional expression and implication in sperm capacitation. Dev Biol 234:261–274. doi: 10.1006/dbio.2001.0196 CrossRefGoogle Scholar
  38. Muschler GF, Nakamoto C, Griffith LG (2004) Engineering principles of clinical cell-based tissue engineering. J Bone Joint Surg Am 86:1541–1558Google Scholar
  39. Musina RA, Bekchanova ES, Belyavskii V (2006) Differentiation potential of mesenchymal stem cells of different origin. Technol Biol Med 2:147–151Google Scholar
  40. Nakagami H, Morishita R, Maeda K, Kikuchi Y, Ogihara T, Kaneda Y (2006) Adipose tissue-derived stromal cells as a novel option for regenerative cell therapy. J Atheroscler Thromb 13:77–81Google Scholar
  41. Nebel RL, Bame JH, Saacke RG, Lim F (1985) Microencapsulation of bovine spermatozoa. J Anim Sci 60(6):1631–1639Google Scholar
  42. Nebel RL, Vishwanath R, McMillan WH, Pitt CJ (1996) Microencapsulation of bovine spermatozoa viability and fertility. Anim Reprod Sci 44:79–89. doi: 10.1016/0378-4320(96)01540-0 CrossRefGoogle Scholar
  43. Nebel RL, Vishwanath R, McMillan WH, Saacke RG (1993) Microencapsulation of bovine spermatozoa for use in artificial insemination: a review. Reprod Fertil Dev 5:701–712. doi: 10.1071/RD9930701 CrossRefGoogle Scholar
  44. O’Halloran D, Pandit AS (2007) Tissue-engineering approach to regenerating the intervertebral disc. Tissue Eng 13:1927–1954. doi: 10.1089/ten.2005.0608 CrossRefGoogle Scholar
  45. Pangas SA, Saudye H, Shea LD, Woodruff TK (2003) Novel approach for the three-dimensional culture of granulose cell-oocyte complexes. Tissue Eng 9:1013–1021. doi: 10.1089/107632703322495655 CrossRefGoogle Scholar
  46. Patrick CW (2000) Adipose tissue engineering: the future of breast and soft tissue reconstruction following tumor resection. Semin Surg Oncol 19:302–311. doi:10.1002/1098-2388(200010/11)19:3<302::AID-SSU12>3.0.CO;2-SCrossRefGoogle Scholar
  47. Patrick CW (2001) Tissue engineering strategies for adipose tissue repair. Anat Rec 263:361–366. doi: 10.1002/ar.1113 CrossRefGoogle Scholar
  48. Richardson SM, Walker RV, Parker S, Rhodes NP, Hunt JA, Freemont AJ, Hoyland JA (2006) Intervertebral disc cell-mediated mesenchymal stem cell differentiation. Stem Cells 24:707–716. doi: 10.1634/stemcells.2005-0205 CrossRefGoogle Scholar
  49. Rigotti G, Marchi A, Galiè M, Baroni G, Benati D, Krampera M, Pasini A, Sbarbati A (2007) Clinical treatment of radiotherapy tissue damage by lipoaspirate transplant: a healing process mediated by adipose-derived adult stem cells. Plast Reconstr Surg 119:1409–1422. doi: 10.1097/01.prs.0000256047.47909.71 CrossRefGoogle Scholar
  50. Rodriguez AM, Elabd C, Delteil F, Astier J, Vernochet C, Saint-Marc P, Guesnet J, Guezennec A, Amri EZ, Dani C, Ailhaud G (2004) Adipocyte differentiation of multipotent cells estabilished from human adipose tissue. Biochem Biophys Res Commun 315:255–263. doi: 10.1016/j.bbrc.2004.01.053 CrossRefGoogle Scholar
  51. Rodriguez AM, Elabd C, Amri E, Ailhaud G, Dani C (2005) The human adipose tissue is a source of multipotent stem cells. Biochimie 87:125–128. doi: 10.1016/j.biochi.2004.11.007 CrossRefGoogle Scholar
  52. Romanov A, Darevskaya A, Merzlikina N (2005) Mesenchymal stem cells from human bone marrow and adipose tissue: isolation, characterization, and differentiation potentialities. Cell Technol Biol Med 3:158–163Google Scholar
  53. Rydèn M, Dicker A, Götherström C, Aström G, Tammik C, Arner P, Le Blanc K (2003) Functional characterization of human mesenchymal stem cell-derived adipocytes. Biochem Biophys Res Commun 14:391–397. doi: 10.1016/j.bbrc.2003.10.010 CrossRefGoogle Scholar
  54. Scherer PE, Williams S, Fogliano M, Baldini G, Lodish HF (1995) A novel serum protein similar to C1q, produced exclusively in adipocytes. J Biol Chem 270:26746–26749. doi: 10.1074/jbc.270.45.26746 CrossRefGoogle Scholar
  55. Strem BM, Hicok KC, Zhu M, Wulur I, Alfonso Z, Schreiber RE, Fraser JK, Hedrick MH (2005) Multipotential differentiation of adipose tissue-derived stem cells. Keio J Med 3:132–141. doi: 10.2302/kjm.54.132 CrossRefGoogle Scholar
  56. Tholpady SS, Llull R, Ogle RC, Rubin JP, Futrell JW, Katz AJ (2006) Adipose tissue: stem cell and beyond. Clin Plast Surg 33:55–62. doi: 10.1016/j.cps.2005.08.004 CrossRefGoogle Scholar
  57. Torre ML (2007) Microincapsulazione di cellule staminali da tessuto adiposo per la terapia rigenerativa di tessuti epiteliali. Acta Vulcanol 5:48–50Google Scholar
  58. Torre ML, Maggi L, Vigo D, Galli A, Bornaghi V, Conte U (2000) Controlled release of swine semen encapsulated in calcium alginate beads. Biomaterials 21:1493–1498. doi: 10.1016/S0142-9612(00)00035-1 CrossRefGoogle Scholar
  59. Torre ML, Munari E, Albani E, Levi-Setti PE, Villani S, Faustini M, Conte U, Vigo D (2006) In vitro maturation of human oocytes in a follicle-mimicking three-dimensional coculture. Fertil Steril 86:572–576. doi: 10.1016/j.fertnstert.2006.02.090 CrossRefGoogle Scholar
  60. Torre ML, Faustini M, Klinger M, Vigo D (2007) Cell encapsulation in reproduction. Recent Patents Drug Deliv Formul 1:85Google Scholar
  61. Uludag H, De-Vos P, Tresco PA (2000) Technology of mammalian cell encapsulation. Adv Drug Deliv Rev 42:29–64. doi: 10.1016/S0169-409X(00)00053-3 CrossRefGoogle Scholar
  62. Vigo D, Torre ML, Faustini M, Munari E, Russo V, Conte U (2005a) I. Capsules containing seminal material for artificial insemination. European Application WO2006106400Google Scholar
  63. Vigo D, Villani S, Faustini M, Accorsi PA, Galeati G, Munari E, Russo V, Asti A, Conte U, Torre ML (2005b) A follicle-like model by granulosa cell encapsulation in a barium alginate/protamine membrane. Tissue Eng 11:709–714. doi: 10.1089/ten.2005.11.709 CrossRefGoogle Scholar
  64. Vigo D, Russo V, Faustini M, Stacchezzini S, Conte U, Torre ML, Accorsi PA, Galeati G, Spinaci M (2006) Preparation of three-dimensional mammalian ovarian follicular cells and ovarian follicle culture systems in a biocompatible matrix. European Patent EP1706103Google Scholar
  65. Villani S, Marazzi M, Bucco M, Faustini M, Klinger M, Gaetani P, Crovato F, Vigo D, Caviggioli F, Torre ML (2008) Statistical approach in alginate membrane formulation for cell encapsulation in a GMP-based cell factory. Acta Biomater 4:943–949. doi: 10.1016/j.actbio.2008.01.007 CrossRefGoogle Scholar
  66. Von Heimburg D, Zachariah S, Heschel I, Kuhuling H, Schoof H, Hafemann B, Paulla N (2001) Human preadypocites seeded on freeze-dried collagen scaffold investigated in vitro and in vivo. Biomaterials 22:429–438. doi: 10.1016/S0142-9612(00)00186-1 CrossRefGoogle Scholar
  67. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372:425–432. doi: 10.1038/372425a0 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Ilaria Ghidoni
    • 1
  • Theodora Chlapanidas
    • 1
  • Massimo Bucco
    • 1
  • Francesca Crovato
    • 2
  • Mario Marazzi
    • 2
  • Daniele Vigo
    • 3
  • Maria Luisa Torre
    • 1
  • Massimo Faustini
    • 3
    Email author
  1. 1.Dipartimento di Chimica FarmaceuticaUniversità di PaviaPaviaItaly
  2. 2.Struttura Semplice Terapia TissutaleAzienda Ospedale Niguarda Ca’ GrandaMilanoItaly
  3. 3.Dipartimento di Scienze e Tecnologie Veterinarie per la Sicurezza AlimentareUniversità di MilanoMilanItaly

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