Advertisement

Stem Cells and Tissue Engineering

  • Troy A. MarkelEmail author
Chapter
Part of the Success in Academic Surgery book series (SIAS)

Abstract

Regenerative medicine deals with the restoration of damaged or injured tissues in patients suffering from catastrophic injuries or chronic diseases in which their own body’s regenerative capacities are not functioning properly. This field typically involves the study of stem cells and the engineering of biological tissues or organs. Stem cells have the unique ability to replicate indefinitely and to differentiate into multiple cells in the body, thereby making them ideal substrates for tissue repair. In this chapter we will examine several facets of regenerative medicine including (1) the types of stem cells available for use, (2) the mechanism of action that these cells use during therapy, and (3) principles of tissue engineering such as scaffolds, bioreactors, and 3D printing.

Keywords

Stem cells Tissue engineering Regenerative medicine 

Notes

Acknowledgment

Disclosure: No disclosures to report.

References

  1. 1.
    Mitalipov S, Wolf D. Totipotency, pluripotency and nuclear reprogramming. Adv Biochem Eng Biotechnol. 2009;114:185–99.PubMedPubMedCentralGoogle Scholar
  2. 2.
    Mitalipov SM, Yeoman RR, Kuo HC, Wolf DP. Monozygotic twinning in rhesus monkeys by manipulation of in vitro-derived embryos. Biol Reprod. 2002;66:1449–55.PubMedCrossRefGoogle Scholar
  3. 3.
    Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981;292:154–6.PubMedCrossRefGoogle Scholar
  4. 4.
    Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A. 1981;78:7634–8.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282:1145–7.CrossRefGoogle Scholar
  6. 6.
    Zhao W, Ji X, Zhang F, Li L, Ma L. Embryonic stem cell markers. Molecules. 2012;17:6196–236.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    President George W. Bush’s address on stem ell research.Google Scholar
  8. 8.
    Obama B. “Executive order 13505 – removing barriers to responsible scientific research involving human stem cells”. Federal Register: Presidental Documents, vol. 74. Washington, DC: The White House; 2009.Google Scholar
  9. 9.
    Wadman M. Stem cells ready for prime time. Nature. 2009;457:516.PubMedCrossRefGoogle Scholar
  10. 10.
    Geron. GRNOPC1 – oligodendrocyte progenitors to address CNS disorders. 2013;2018.Google Scholar
  11. 11.
    Cyranoski D. Trials of embryonic stem cells to launch in China. Nature. 2017;546:15–6.PubMedCrossRefGoogle Scholar
  12. 12.
    Civin CI, Strauss LC, Brovall C, Fackler MJ, Schwartz JF, Shaper JH. Antigenic analysis of hematopoiesis. III. A hematopoietic progenitor cell surface antigen defined by a monoclonal antibody raised against KG-1a cells. J Immunol. 1984;133:157–65.PubMedGoogle Scholar
  13. 13.
    Jacobson LO, Simmons EL, Marks EK, Eldredge JH. Recovery from radiation injury. Science. 1951;113:510–1.PubMedCrossRefGoogle Scholar
  14. 14.
    Eaves CJ. Hematopoietic stem cells: concepts, definitions, and the new reality. Blood. 2015;125:2605–13.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Jacobsohn DA, Loken MR, Fei M, Adams A, Brodersen LE, Logan BR, Ahn KW, Shaw BE, Kletzel M, Olszewski M, Khan S, Meshinchi S, Keating A, Harris A, Teira P, Duerst RE, Margossian SP, Martin PL, Petrovic A, Dvorak CC, Nemecek ER, Boyer MW, Chen AR, Davis JH, Shenoy S, Savasan S, Hudspeth MP, Adams RH, Lewis VA, Kheradpour A, Kasow KA, Gillio AP, Haight AE, Bhatia M, Bambach BJ, Haines HL, Quigg TC, Greiner RJ, Talano JM, Delgado DC, Cheerva A, Gowda M, Ahuja S, Ozkaynak M, Mitchell D, Schultz KR, Fry TJ, Loeb DM, Pulsipher MA. Outcomes of measurable residual disease in pediatric acute myeloid leukemia before and after hematopoietic stem cell transplant: validation of difference from normal flow cytometry with chimerism studies and wilms tumor 1 gene expression. Biol Blood Marrow Transplant. 2018;24(10):2040–6.PubMedCrossRefGoogle Scholar
  16. 16.
    Itonaga H, Kato T, Fujioka M, Taguchi M, Taniguchi H, Imaizumi Y, Yoshida S, Miyoshi H, Moriuchi Y, Ohshima K, Miyazaki Y. High-dose chemotherapy with stem cell rescue provided durable remission for classical hodgkin lymphoma-type post-transplant lymphoproliferative disorder after unrelated cord blood transplantation: a case report and review of the literature. Intern Med. 2017;56:1873–7.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Kassim AA, Sharma D. Hematopoietic stem cell transplantation for sickle cell disease: the changing landscape. Hematol Oncol Stem Cell Ther. 2017;10:259–66.PubMedCrossRefGoogle Scholar
  18. 18.
    Jaing TH. Is the benefit-risk ratio for patients with transfusion-dependent thalassemia treated by unrelated cord blood transplantation favorable? Int J Mol Sci. 2017;18:pii:E2472.CrossRefGoogle Scholar
  19. 19.
    Charbord P. Bone marrow mesenchymal stem cells: historical overview and concepts. Hum Gene Ther. 2010;21:1045–56.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Mahla RS. Stem cells applications in regenerative medicine and disease therapeutics. Int J Cell Biol. 2016;2016:6940283.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Jensen AR, Manning MM, Khaneki S, Drucker NA, Markel TA. Harvest tissue source does not alter the protective power of stromal cell therapy after intestinal ischemia and reperfusion injury. J Surg Res. 2016;204:361–70.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Doster DL, Jensen AR, Khaneki S, Markel TA. Mesenchymal stromal cell therapy for the treatment of intestinal ischemia: defining the optimal cell isolate for maximum therapeutic benefit. Cytotherapy. 2016;18:1457–70.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Clinical Trials. 2018: Search for “mesenchymal stem cells”; 2018.Google Scholar
  24. 24.
    Androutsellis-Theotokis A, Rueger MA, Park DM, Mkhikian H, Korb E, Poser SW, Walbridge S, Munasinghe J, Koretsky AP, Lonser RR, McKay RD. Targeting neural precursors in the adult brain rescues injured dopamine neurons. Proc Natl Acad Sci U S A. 2009;106:13570–5.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Taverna E, Gotz M, Huttner WB. The cell biology of neurogenesis: toward an understanding of the development and evolution of the neocortex. Annu Rev Cell Dev Biol. 2014;30:465–502.PubMedCrossRefGoogle Scholar
  26. 26.
    Paspala SA, Murthy TV, Mahaboob VS, Habeeb MA. Pluripotent stem cells – a review of the current status in neural regeneration. Neurol India. 2011;59:558–65.PubMedCrossRefGoogle Scholar
  27. 27.
    Pruszak J, Ludwig W, Blak A, Alavian K, Isacson O. CD15, CD24, and CD29 define a surface biomarker code for neural lineage differentiation of stem cells. Stem Cells. 2009;27:2928–40.PubMedPubMedCentralGoogle Scholar
  28. 28.
    Stamp LA. Cell therapy for GI motility disorders: comparison of cell sources and proposed steps for treating Hirschsprung disease. Am J Physiol Gastrointest Liver Physiol. 2017;312:G348–54.PubMedCrossRefGoogle Scholar
  29. 29.
    Cheng LS, Hotta R, Graham HK, Belkind-Gerson J, Nagy N, Goldstein AM. Postnatal human enteric neuronal progenitors can migrate, differentiate, and proliferate in embryonic and postnatal aganglionic gut environments. Pediatr Res. 2017;81:838–46.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Kayahara T, Sawada M, Takaishi S, Fukui H, Seno H, Fukuzawa H, Suzuki K, Hiai H, Kageyama R, Okano H, Chiba T. Candidate markers for stem and early progenitor cells, Musashi-1 and Hes1, are expressed in crypt base columnar cells of mouse small intestine. FEBS Lett. 2003;535:131–5.PubMedCrossRefGoogle Scholar
  31. 31.
    Booth C, Potten CS. Gut instincts: thoughts on intestinal epithelial stem cells. J Clin Invest. 2000;105:1493–9.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Barker N, van Oudenaarden A, Clevers H. Identifying the stem cell of the intestinal crypt: strategies and pitfalls. Cell Stem Cell. 2012;11:452–60.PubMedCrossRefGoogle Scholar
  33. 33.
    Carmon KS, Gong X, Lin Q, Thomas A, Liu Q. R-Spondins function as ligands of the orphan receptors LGR4 and LGR5 to regulate Wnt/beta-catenin signaling. Proc Natl Acad Sci U S A. 2011;108:11452–7.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Itzkovitz S, Lyubimova A, Blat IC, Maynard M, van Es J, Lees J, Jacks T, Clevers H, van Oudenaarden A. Single-molecule transcript counting of stem-cell markers in the mouse intestine. Nat Cell Biol. 2011;14:106–14.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Munoz J, Stange DE, Schepers AG, van de Wetering M, Koo BK, Itzkovitz S, Volckmann R, Kung KS, Koster J, Radulescu S, Myant K, Versteeg R, Sansom OJ, van Es JH, Barker N, van Oudenaarden A, Mohammed S, Heck AJ, Clevers H. The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent ‘+4’ cell markers. EMBO J. 2012;31:3079–91.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Tian H, Biehs B, Warming S, Leong KG, Rangell L, Klein OD, de Sauvage FJ. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature. 2011;478:255–9.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Miyajima A, Tanaka M, Itoh T. Stem/progenitor cells in liver development, homeostasis, regeneration, and reprogramming. Cell Stem Cell. 2014;14:561–74.PubMedCrossRefGoogle Scholar
  38. 38.
    Suzuki A, Zheng Y, Kondo R, Kusakabe M, Takada Y, Fukao K, Nakauchi H, Taniguchi H. Flow-cytometric separation and enrichment of hepatic progenitor cells in the developing mouse liver. Hepatology. 2000;32:1230–9.PubMedCrossRefGoogle Scholar
  39. 39.
    Tanimizu N, Nishikawa M, Saito H, Tsujimura T, Miyajima A. Isolation of hepatoblasts based on the expression of Dlk/Pref-1. J Cell Sci. 2003;116:1775–86.PubMedCrossRefGoogle Scholar
  40. 40.
    Nitou M, Sugiyama Y, Ishikawa K, Shiojiri N. Purification of fetal mouse hepatoblasts by magnetic beads coated with monoclonal anti-e-cadherin antibodies and their in vitro culture. Exp Cell Res. 2002;279:330–43.PubMedCrossRefGoogle Scholar
  41. 41.
    Nierhoff D, Ogawa A, Oertel M, Chen YQ, Shafritz DA. Purification and characterization of mouse fetal liver epithelial cells with high in vivo repopulation capacity. Hepatology. 2005;42:130–9.PubMedCrossRefGoogle Scholar
  42. 42.
    Watanabe T, Nakagawa K, Ohata S, Kitagawa D, Nishitai G, Seo J, Tanemura S, Shimizu N, Kishimoto H, Wada T, Aoki J, Arai H, Iwatsubo T, Mochita M, Watanabe T, Satake M, Ito Y, Matsuyama T, Mak TW, Penninger JM, Nishina H, Katada T. SEK1/MKK4-mediated SAPK/JNK signaling participates in embryonic hepatoblast proliferation via a pathway different from NF-kappaB-induced anti-apoptosis. Dev Biol. 2002;250:332–47.PubMedCrossRefGoogle Scholar
  43. 43.
    Schmelzer E, Zhang L, Bruce A, Wauthier E, Ludlow J, Yao HL, Moss N, Melhem A, McClelland R, Turner W, Kulik M, Sherwood S, Tallheden T, Cheng N, Furth ME, Reid LM. Human hepatic stem cells from fetal and postnatal donors. J Exp Med. 2007;204:1973–87.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K, Leri A, Kajstura J, Nadal-Ginard B, Anversa P. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell. 2003;114:763–76.PubMedCrossRefGoogle Scholar
  45. 45.
    Messina E, De Angelis L, Frati G, Morrone S, Chimenti S, Fiordaliso F, Salio M, Battaglia M, Latronico MV, Coletta M, Vivarelli E, Frati L, Cossu G, Giacomello A. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res. 2004;95:911–21.PubMedCrossRefGoogle Scholar
  46. 46.
    Miyamoto S, Kawaguchi N, Ellison GM, Matsuoka R, Shin’oka T, Kurosawa H. Characterization of long-term cultured c-kit+ cardiac stem cells derived from adult rat hearts. Stem Cells Dev. 2010;19:105–16.PubMedCrossRefGoogle Scholar
  47. 47.
    Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y, Pocius J, Michael LH, Behringer RR, Garry DJ, Entman ML, Schneider MD. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A. 2003;100:12313–8.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Bolli R, Chugh AR, D’Amario D, Loughran JH, Stoddard MF, Ikram S, Beache GM, Wagner SG, Leri A, Hosoda T, Sanada F, Elmore JB, Goichberg P, Cappetta D, Solankhi NK, Fahsah I, Rokosh DG, Slaughter MS, Kajstura J, Anversa P. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet. 2011;378:1847–57.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Chugh AR, Beache GM, Loughran JH, Mewton N, Elmore JB, Kajstura J, Pappas P, Tatooles A, Stoddard MF, Lima JA, Slaughter MS, Anversa P, Bolli R. Administration of cardiac stem cells in patients with ischemic cardiomyopathy: the SCIPIO trial: surgical aspects and interim analysis of myocardial function and viability by magnetic resonance. Circulation. 2012;126:S54–64.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Keith MC, Tang XL, Tokita Y, Li QH, Ghafghazi S, Moore Iv J, Hong KU, Elmore B, Amraotkar A, Ganzel BL, Grubb KJ, Flaherty MP, Hunt G, Vajravelu B, Wysoczynski M, Bolli R. Safety of intracoronary infusion of 20 million C-kit positive human cardiac stem cells in pigs. PLoS One. 2015;10:e0124227.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Leong YY, Ng WH, Ellison-Hughes GM, Tan JJ. Cardiac stem cells for myocardial regeneration: they are not alone. Front Cardiovasc Med. 2017;4:47.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Makkar RR, Smith RR, Cheng K, Malliaras K, Thomson LE, Berman D, Czer LS, Marban L, Mendizabal A, Johnston PV, Russell SD, Schuleri KH, Lardo AC, Gerstenblith G, Marban E. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet. 2012;379:895–904.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–76.CrossRefGoogle Scholar
  54. 54.
    Malik N, Rao MS. A review of the methods for human iPSC derivation. Methods Mol Biol. 2013;997:23–33.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Yannarelli G, Tsoporis JN, Desjardins JF, Wang XH, Pourdjabbar A, Viswanathan S, Parker TG, Keating A. Donor mesenchymal stromal cells (MSCs) undergo variable cardiac reprogramming in vivo and predominantly co-express cardiac and stromal determinants after experimental acute myocardial infarction. Stem Cell Rev. 2014;10:304–15.PubMedCrossRefGoogle Scholar
  56. 56.
    Morigi M, Imberti B, Zoja C, Corna D, Tomasoni S, Abbate M, Rottoli D, Angioletti S, Benigni A, Perico N, Alison M, Remuzzi G. Mesenchymal stem cells are renotropic, helping to repair the kidney and improve function in acute renal failure. J Am Soc Nephrol. 2004;15:1794–804.PubMedCrossRefGoogle Scholar
  57. 57.
    Sasaki M, Abe R, Fujita Y, Ando S, Inokuma D, Shimizu H. Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell type. J Immunol. 2008;180:2581–7.PubMedCrossRefGoogle Scholar
  58. 58.
    Liu L, Chiu PW, Lam PK, Poon CC, Lam CC, Ng EK, Lai PB. Effect of local injection of mesenchymal stem cells on healing of sutured gastric perforation in an experimental model. Br J Surg. 2015;102:e158–68.PubMedCrossRefGoogle Scholar
  59. 59.
    Rojas M, Xu J, Woods CR, Mora AL, Spears W, Roman J, Brigham KL. Bone marrow-derived mesenchymal stem cells in repair of the injured lung. Am J Respir Cell Mol Biol. 2005;33:145–52.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Kotton DN, Ma BY, Cardoso WV, Sanderson EA, Summer RS, Williams MC, Fine A. Bone marrow-derived cells as progenitors of lung alveolar epithelium. Development. 2001;128:5181–8.PubMedGoogle Scholar
  61. 61.
    Crisostomo PR, Markel TA, Wang M, Lahm T, Lillemoe KD, Meldrum DR. In the adult mesenchymal stem cell population, source gender is a biologically relevant aspect of protective power. Surgery. 2007;142:215–21.PubMedCrossRefGoogle Scholar
  62. 62.
    Crisostomo PR, Wang M, Markel TA, Lahm T, Abarbanell AM, Herrmann JL, Meldrum DR. Stem cell mechanisms and paracrine effects: potential in cardiac surgery. Shock. 2007;28:375–83.PubMedCrossRefGoogle Scholar
  63. 63.
    Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM, Fike JR, Lee HO, Pfeffer K, Lois C, Morrison SJ, Alvarez-Buylla A. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature. 2003;425:968–73.PubMedCrossRefGoogle Scholar
  64. 64.
    Mishra PJ, Mishra PJ, Banerjee D. Cell-free derivatives from mesenchymal stem cells are effective in wound therapy. World J Stem Cells. 2012;4:35–43.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Cantinieaux D, Quertainmont R, Blacher S, Rossi L, Wanet T, Noel A, Brook G, Schoenen J, Franzen R. Conditioned medium from bone marrow-derived mesenchymal stem cells improves recovery after spinal cord injury in rats: an original strategy to avoid cell transplantation. PLoS One. 2013;8:e69515.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Dreixler JC, Poston JN, Balyasnikova I, Shaikh AR, Tupper KY, Conway S, Boddapati V, Marcet MM, Lesniak MS, Roth S. Delayed administration of bone marrow mesenchymal stem cell conditioned medium significantly improves outcome after retinal ischemia in rats. Invest Ophthalmol Vis Sci. 2014;55:3785–96.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Nakano N, Nakai Y, Seo TB, Yamada Y, Ohno T, Yamanaka A, Nagai Y, Fukushima M, Suzuki Y, Nakatani T, Ide C. Characterization of conditioned medium of cultured bone marrow stromal cells. Neurosci Lett. 2010;483:57–61.PubMedCrossRefGoogle Scholar
  68. 68.
    Weil BR, Markel TA, Herrmann JL, Abarbanell AM, Meldrum DR. Mesenchymal stem cells enhance the viability and proliferation of human fetal intestinal epithelial cells following hypoxic injury via paracrine mechanisms. Surgery. 2009;146:190–7.PubMedCrossRefGoogle Scholar
  69. 69.
    Crisostomo PR, Markel TA, Wang Y, Meldrum DR. Surgically relevant aspects of stem cell paracrine effects. Surgery. 2008;143:577–81.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Lee RH, Pulin AA, Seo MJ, Kota DJ, Ylostalo J, Larson BL, Semprun-Prieto L, Delafontaine P, Prockop DJ. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell. 2009;5:54–63.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Walker PA, Shah SK, Jimenez F, Aroom KR, Harting MT, Cox CS Jr. Bone marrow-derived stromal cell therapy for traumatic brain injury is neuroprotective via stimulation of non-neurologic organ systems. Surgery. 2012;152:790–3.PubMedCrossRefGoogle Scholar
  72. 72.
    Walker PA, Shah SK, Jimenez F, Gerber MH, Xue H, Cutrone R, Hamilton JA, Mays RW, Deans R, Pati S, Dash PK, Cox CS Jr. Intravenous multipotent adult progenitor cell therapy for traumatic brain injury: preserving the blood brain barrier via an interaction with splenocytes. Exp Neurol. 2010;225:341–52.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, de Gruijl TD, Wurdinger T, Middeldorp JM. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci U S A. 2010;107:6328–33.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Shabbir A, Cox A, Rodriguez-Menocal L, Salgado M, Van Badiavas E. Mesenchymal stem cell exosomes induce proliferation and migration of normal and chronic wound fibroblasts, and enhance angiogenesis in vitro. Stem Cells Dev. 2015;24:1635–47.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Tomasoni S, Longaretti L, Rota C, Morigi M, Conti S, Gotti E, Capelli C, Introna M, Remuzzi G, Benigni A. Transfer of growth factor receptor mRNA via exosomes unravels the regenerative effect of mesenchymal stem cells. Stem Cells Dev. 2013;22:772–80.PubMedCrossRefGoogle Scholar
  76. 76.
    Nichols TC. NF-kappaB and reperfusion injury. Drug News Perspect. 2004;17:99–104.PubMedCrossRefGoogle Scholar
  77. 77.
    Jiang H, Qu L, Dou R, Lu L, Bian S, Zhu W. Potential role of mesenchymal stem cells in alleviating intestinal ischemia/reperfusion impairment. PLoS One. 2013;8:e74468.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Tanaka F, Tominaga K, Ochi M, Tanigawa T, Watanabe T, Fujiwara Y, Ohta K, Oshitani N, Higuchi K, Arakawa T. Exogenous administration of mesenchymal stem cells ameliorates dextran sulfate sodium-induced colitis via anti-inflammatory action in damaged tissue in rats. Life Sci. 2008;83:771–9.PubMedCrossRefGoogle Scholar
  79. 79.
    Maggini J, Mirkin G, Bognanni I, Holmberg J, Piazzón IM, Nepomnaschy I, Costa H, Cañones C, Raiden S, Vermeulen M, Geffner JR. Mouse bone marrow-derived mesenchymal stromal cells turn activated macrophages into a regulatory-like profile. PLoS One. 2010;5:e9252.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Singer NG, Caplan AI. Mesenchymal stem cells: mechanisms of inflammation. Annu Rev Pathol. 2011;6:457–78.PubMedCrossRefGoogle Scholar
  81. 81.
    Beyth S, Borovsky Z, Mevorach D, Liebergall M, Gazit Z, Aslan H, Galun E, Rachmilewitz J. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood. 2005;105:2214–9.PubMedCrossRefGoogle Scholar
  82. 82.
    Tolar J, Le Blanc K, Keating A, Blazar BR. Hitting the right spot with mesenchymal stromal cells (MSCs). Stem cells (Dayton, OH). 2010;28:1446–55.CrossRefGoogle Scholar
  83. 83.
    Nemeth K, Leelahavanichkul A, Yuen PS, Mayer B, Parmelee A, Doi K, Robey PG, Leelahavanichkul K, Koller BH, Brown JM, Hu X, Jelinek I, Star RA, Mezey E. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med. 2009;15:42–9.PubMedCrossRefGoogle Scholar
  84. 84.
    Melief SM, Geutskens SB, Fibbe WE, Roelofs H. Multipotent stromal cells skew monocytes towards an anti-inflammatory interleukin-10-producing phenotype by production of interleukin-6. Haematologica. 2013;98:888–95.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Lin CM, Gu J, Zhang Y, Shen LJ, Ma L, Ni J, Wang ZQ, Wu W. Effect of UC-MSCs on inflammation and thrombosis of the rats with collagen type II induced arthritis. Zhongh Xuey Zazhi. 2012;33:215–9.Google Scholar
  86. 86.
    Kinnaird T, Stabile E, Burnett MS, Lee CW, Barr S, Fuchs S, Epstein SE. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res. 2004;94:678–85.PubMedCrossRefGoogle Scholar
  87. 87.
    Wang M, Crisostomo PR, Herring C, Meldrum KK, Meldrum DR. Human progenitor cells from bone marrow or adipose tissue produce VEGF, HGF, and IGF-I in response to TNF by a p38 MAPK-dependent mechanism. Am J Physiol Regul Integr Comp Physiol. 2006;291:R880–4.PubMedCrossRefGoogle Scholar
  88. 88.
    Markel TA, Wang Y, Herrmann JL, Crisostomo PR, Wang M, Novotny NM, Herring CM, Tan J, Lahm T, Meldrum DR. VEGF is critical for stem cell-mediated cardioprotection and a crucial paracrine factor for defining the age threshold in adult and neonatal stem cell function. Am J Physiol Heart Circ Physiol. 2008;295:H2308–14.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Crafts TD, Jensen AR, Blocher-Smith EC, Markel TA. Vascular endothelial growth factor: therapeutic possibilities and challenges for the treatment of ischemia. Cytokine. 2015;71:385–93.PubMedCrossRefGoogle Scholar
  90. 90.
    Kinnaird T, Stabile E, Burnett MS, Shou M, Lee CW, Barr S, Fuchs S, Epstein SE. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation. 2004;109:1543–9.PubMedCrossRefGoogle Scholar
  91. 91.
    Gerber HP, Malik AK, Solar GP, Sherman D, Liang XH, Meng G, Hong K, Marsters JC, Ferrara N. VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature. 2002;417:954–8.PubMedCrossRefGoogle Scholar
  92. 92.
    Zhang JC, Zheng GF, Wu L, Ou Yang LY, Li WX. Bone marrow mesenchymal stem cells overexpressing human basic fibroblast growth factor increase vasculogenesis in ischemic rats. Braz J Med Biol Res. 2014;47:886–94.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Zhang W, Shen ZY, Song HL, Yang Y, Wu BJ, Fu NN, Liu T. Protective effect of bone marrow mesenchymal stem cells in intestinal barrier permeability after heterotopic intestinal transplantation. World J Gastroenterol. 2014;20:7442–51.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Dernbach E, Urbich C, Brandes RP, Hofmann WK, Zeiher AM, Dimmeler S. Antioxidative stress-associated genes in circulating progenitor cells: evidence for enhanced resistance against oxidative stress. Blood. 2004;104:3591–7.PubMedCrossRefGoogle Scholar
  95. 95.
    Valle-Prieto A, Conget PA. Human mesenchymal stem cells efficiently manage oxidative stress. Stem Cells Dev. 2010;19:1885–93.PubMedCrossRefGoogle Scholar
  96. 96.
    Howard D, Buttery LD, Shakesheff KM, Roberts SJ. Tissue engineering: strategies, stem cells and scaffolds. J Anat. 2008;213:66–72.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Yang S, Leong KF, Du Z, Chua CK. The design of scaffolds for use in tissue engineering. Part I traditional factors. Tissue Eng. 2001;7:679–89.PubMedCrossRefGoogle Scholar
  98. 98.
    de la Puente P, Ludena D. Cell culture in autologous fibrin scaffolds for applications in tissue engineering. Exp Cell Res. 2014;322:1–11.PubMedCrossRefGoogle Scholar
  99. 99.
    Kanczler JM, Barry J, Ginty P, Howdle SM, Shakesheff KM, Oreffo RO. Supercritical carbon dioxide generated vascular endothelial growth factor encapsulated poly(DL-lactic acid) scaffolds induce angiogenesis in vitro. Biochem Biophys Res Commun. 2007;352:135–41.PubMedCrossRefGoogle Scholar
  100. 100.
    Chen YW, Chiou SH, Wong TT, Ku HH, Lin HT, Chung CF, Yen SH, Kao CL. Using gelatin scaffold with coated basic fibroblast growth factor as a transfer system for transplantation of human neural stem cells. Transplant Proc. 2006;38:1616–7.PubMedCrossRefGoogle Scholar
  101. 101.
    Suciati T, Howard D, Barry J, Everitt NM, Shakesheff KM, Rose FR. Zonal release of proteins within tissue engineering scaffolds. J Mater Sci Mater Med. 2006;17:1049–56.PubMedCrossRefGoogle Scholar
  102. 102.
    Barry JJA, Howard D, Shakesheff KM, Howdle SM, Alexander MR. Using a core-sheath distribution of chemistry through tissue engineering scaffolds to control cell ingress. Adv Mater. 2006;18:1406–10.CrossRefGoogle Scholar
  103. 103.
    Stephenson M, Grayson W. Recent advances in bioreactors for cell-based therapies. F1000Res. 2018;7:F1000 Faculty Rev-517.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Shekaran A, Lam A, Sim E, Jialing L, Jian L, Wen JT, Chan JK, Choolani M, Reuveny S, Birch W, Oh S. Biodegradable ECM-coated PCL microcarriers support scalable human early MSC expansion and in vivo bone formation. Cytotherapy. 2016;18:1332–44.PubMedCrossRefGoogle Scholar
  105. 105.
    Wang Y, Cheng L, Gerecht S. Efficient and scalable expansion of human pluripotent stem cells under clinically compliant settings: a view in 2013. Ann Biomed Eng. 2014;42:1357–72.PubMedCrossRefGoogle Scholar
  106. 106.
    Stucki AO, Stucki JD, Hall SR, Felder M, Mermoud Y, Schmid RA, Geiser T, Guenat OT. A lung-on-a-chip array with an integrated bio-inspired respiration mechanism. Lab Chip. 2015;15:1302–10.PubMedCrossRefGoogle Scholar
  107. 107.
    Benam KH, Villenave R, Lucchesi C, Varone A, Hubeau C, Lee HH, Alves SE, Salmon M, Ferrante TC, Weaver JC, Bahinski A, Hamilton GA, Ingber DE. Small airway-on-a-chip enables analysis of human lung inflammation and drug responses in vitro. Nat Methods. 2016;13:151–7.PubMedCrossRefGoogle Scholar
  108. 108.
    Zhang B, Montgomery M, Chamberlain MD, Ogawa S, Korolj A, Pahnke A, Wells LA, Masse S, Kim J, Reis L, Momen A, Nunes SS, Wheeler AR, Nanthakumar K, Keller G, Sefton MV, Radisic M. Biodegradable scaffold with built-in vasculature for organ-on-a-chip engineering and direct surgical anastomosis. Nat Mater. 2016;15:669–78.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    van Kogelenberg S, Yue Z, Dinoro JN, Baker CS, Wallace GG. Three-dimensional printing and cell therapy for wound repair. Adv Wound Care. 2018;7:145–55.CrossRefGoogle Scholar
  110. 110.
    Unger C, Gruene M, Kock L, Kock J, Chichkov BN. Time-resolved imaging of hydrogel printing via laser-induced forward transfer. Appl Phys A. 2011;103:271–7.CrossRefGoogle Scholar
  111. 111.
    Schmidt W. The use of diodes for daily quality assurance on radiotherapy equipment. Radiobiol Radiother. 1990;31:155–60.Google Scholar
  112. 112.
    Jammalamadaka U, Tappa K. Recent advances in biomaterials for 3D printing and tissue engineering. J Funct Biomater. 2018;9:pii: E22.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Section of Pediatric Surgery, Department of Surgery, Riley Hospital for Children at Indiana University HealthThe Indiana University School of MedicineIndianapolisUSA

Personalised recommendations