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Engineering Integrative Stem Cell and Biomaterial Therapies for Peripheral Artery Disease

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Part of the book series: Biosystems & Biorobotics ((BIOSYSROB,volume 9))

Abstract

Because of their potential to regenerate tissues and organs, stem cells garner extensive interest worldwide for treating a wide range of degenerative diseases. In numerous efforts, a variety of stem cell formats have been considered for therapeutic purposes to combat such pathologies, one being vascular-related diseases. In particular, the prevalence of peripheral artery disease (PAD) has steadily increased with the growth of the aging population in many first-world countries. Considering this disturbing trend as well as the obesity epidemic and the ballooning population growth in third-world nations, the burden of PAD is expected to increase worldwide to alarming levels in the coming decades. The advent of stem cell treatments could stymie this burden by alleviating the complications and improving upon the less-than-satisfactory outcomes from current standard-of-care surgical/pharmacological interventions for PAD. This chapter reviews the relevant, cutting-edge clinical and animal model research efforts in the field and explores the remaining questions as they pertain to convergence technologies that may provide the potential for stem cells to reverse PAD-induced tissue damage. Harnessing and translating this potential to create more viable and efficacious PAD treatments should be of paramount global and public health concern.

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References

  1. Botman, O., Wyns, C.: Induced pluripotent stem cell potential in medicine, specifically focused on reproductive medicine. Frontiers in Surgery 1, 5 (2014)

    Google Scholar 

  2. Singh, V.K., Kalsan, M., Kumar, N., Saini, A., Chandra, R.: Induced pluripotent stem cells: Applications in regenerative medicine, disease modeling, and drug discovery. Frontiers in Cell and Developmental Biology 3, 2 (2015)

    Google Scholar 

  3. Fowkes, F.G., Rudan, D., Rudan, I., Aboyans, V., Denenberg, J.O., McDermott, M.M., Norman, P.E., Sampson, U.K., Williams, L.J., Mensah, G.A., Criqui, M.H.: Comparison of global estimates of prevalence and risk factors for peripheral artery disease in 2000 and 2010: A systematic review and analysis. Lancet 382, 1329–1340 (2013)

    Google Scholar 

  4. Hirsch, A.T., Hartman, L., Town, R.J., Virnig, B.A.: National health care costs of peripheral arterial disease in the medicare population. Vasc. Med. 13, 209–215 (2008)

    Google Scholar 

  5. Mahoney, E.M., Wang, K., Keo, H.H., Duval, S., Smolderen, K.G., Cohen, D.J., Steg, G., Bhatt, D.L., Hirsch, A.T.: Reduction of Atherothrombosis for Continued Health Registry I. Vascular hospitalization rates and costs in patients with peripheral artery disease in the united states. Circulation. Cardiovascular Quality and Outcomes 3, 642–651 (2010)

    Google Scholar 

  6. Olin, J.W., Sealove, B.A.: Peripheral artery disease: Current insight into the disease and its diagnosis and management. Mayo Clin. Proc. 85, 678–692 (2010)

    Google Scholar 

  7. Mueller-Schweinitzer, E., Muller, S.E., Reineke, D.C., Kern, T., Carrel, T.P., Eckstein, F.S., Grapow, M.T.R.: Reactive oxygen species mediate functional differences in human radial and internal thoracic arteries from smokers. J. Vasc. Surg. 51, 438–444 (2010)

    Google Scholar 

  8. Jude, E.B., Eleftheriadou, I., Tentolouris, N.: Peripheral arterial disease in diabetes–a review. Diabet. Med. 27, 4–14 (2010)

    Google Scholar 

  9. Boyette, L.B., Tuan, R.S.: Adult stem cells and diseases of aging. Journal of Clinical Medicine 3, 88–134 (2014)

    Google Scholar 

  10. Challen, G.A., Little, M.H.: A side order of stem cells: The sp phenotype. Stem Cells 24, 3–12 (2006)

    Google Scholar 

  11. Salem, H.K., Thiemermann, C.: Mesenchymal stromal cells: Current understanding and clinical status. Stem Cells 28, 585–596 (2010)

    Google Scholar 

  12. Friedenstein, A.J., Petrakova, K.V., Kurolesova, A.I., Frolova, G.P.: Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 6, 230–247 (1968)

    Google Scholar 

  13. Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswal, R.K., Douglas, R., Mosca, J.D., Moorman, M.A., Simonetti, D.W., Craig, S., Marshak, D.R.: Multilineage potential of adult human mesenchymal stem cells. Science 284, 143–147 (1999)

    Google Scholar 

  14. Asahara, T., Masuda, H., Takahashi, T., Kalka, C., Pastore, C., Silver, M., Kearne, M., Magner, M., Isner, J.M.: Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circulation Research 85, 221–228 (1999)

    Google Scholar 

  15. Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T., Witzenbichler, B., Schatteman, G., Isner, J.M.: Isolation of Putative Progenitor Endothelial Cells for Angiogenesis. Science 275, 964–967 (1997)

    Google Scholar 

  16. Kalka, C., Masuda, H., Takahashi, T., Kalka-Moll, W.M., Silver, M., Kearney, M., Li, T., Isner, J.M., Asahara, T.: Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc. Natl. Acad Sci. USA 97, 3422–3427 (2000)

    Google Scholar 

  17. Rehman, J., Li, J., Orschell, C.M., March, K.L.: Peripheral blood “endothelial progenitor cells” are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 107, 1164–1169 (2003)

    Google Scholar 

  18. Caballero, S., Sengupta, N., Afzal, A., Chang, K.H., Li Calzi, S., Guberski, D.L., Kern, T.S., Grant, M.B.: Ischemic vascular damage can be repaired by healthy, but not diabetic, endothelial progenitor cells. Diabetes 56, 960–967 (2007)

    Google Scholar 

  19. Oswald, J., Boxberger, S., Jørgensen, B., Feldmann, S., Ehninger, G., Bornhäuser, M., Werner, C.: Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22, 377–384 (2004)

    Google Scholar 

  20. Silva, G.V., Litovsky, S., Assad, J.A., Sousa, A.L., Martin, B.J., Vela, D., Coulter, S.C., Lin, J., Ober, J., Vaughn, W.K.: Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Circulation 111, 150–156 (2005)

    Google Scholar 

  21. Uccelli, A., Moretta, L., Pistoia, V.: Mesenchymal stem cells in health and disease. Nature Reviews. Immunology 8, 726–736 (2008)

    Google Scholar 

  22. Shantsila, E., Watson, T., Tse, H.F., Lip, G.Y.: New insights on endothelial progenitor cell subpopulations and their angiogenic properties. J. Am. Coll. Cardiol. 51, 669–671 (2008)

    Google Scholar 

  23. Gao, L., Chen, Q., Zhou, X., Fan, L.: The role of hypoxia-inducible factor 1 in atherosclerosis. Journal of Clinical Pathology (2012)

    Google Scholar 

  24. Selvin, E., Erlinger, T.P.: Prevalence of and risk factors for peripheral arterial disease in the united states: Results from the national health and nutrition examination survey, 1999-2000. Circulation 110, 738–743 (2004)

    Google Scholar 

  25. Sanz, J., Fayad, Z.A.: Imaging of atherosclerotic cardiovascular disease. Nature 451, 953–957 (2008)

    Google Scholar 

  26. Sluimer, J.C., Daemen, M.J.: Novel concepts in atherogenesis: Angiogenesis and hypoxia in atherosclerosis. J. Pathol. 218, 7–29 (2009)

    Google Scholar 

  27. Gao, L., Chen, Q., Zhou, X., Fan, L.: The role of hypoxia-inducible factor 1 in atherosclerosis. Journal of Clinical Pathology 65, 872–876 (2012)

    Google Scholar 

  28. Golomb, B.A., Dang, T.T., Criqui, M.H.: Peripheral arterial disease: Morbidity and mortality implications. Circulation 114, 688–699 (2006)

    Google Scholar 

  29. Bhatt, D.L., Flather, M.D., Hacke, W., Berger, P.B., Black, H.R., Boden, W.E., Cacoub, P., Cohen, E.A., Creager, M.A., Easton, J.D., Hamm, C.W., Hankey, G.J., Johnston, S.C., Mak, K.H., Mas, J.L., Montalescot, G., Pearson, T.A., Steg, P.G., Steinhubl, S.R., Weber, M.A., Fabry-Ribaudo, L., Hu, T., Topol, E.J., Fox, K.A.: Patients with prior myocardial infarction, stroke, or symptomatic peripheral arterial disease in the charisma trial. J. Am. Coll. Cardiol. 49, 1982–1988 (2007)

    Google Scholar 

  30. Mrc/bhf heart protection study of cholesterol lowering with simvastatin in 20,536 high-risk individuals: A randomised placebo-controlled trial. Lancet 360, 7–22 (2002)

    Google Scholar 

  31. Garcia, L.A., Lyden, S.P.: Atherectomy for infrainguinal peripheral artery disease. J. Endovasc. Ther. 16(II), 105–115 (2009)

    Google Scholar 

  32. Collinson, D.J., Donnelly, R.: Therapeutic angiogenesis in peripheral arterial disease: Can biotechnology produce an effective collateral circulation? European Journal of Vascular and Endovascular Surgery: the Official Journal of the European Society for Vascular Surgery 28, 9–23 (2004)

    Google Scholar 

  33. Berger, J.S., Krantz, M.J., Kittelson, J.M., Hiatt, W.R.: Aspirin for the prevention of cardiovascular events in patients with peripheral artery disease: A meta-analysis of randomized trials. Jama 301, 1909–1919 (2009)

    Google Scholar 

  34. Kalka, C., Baumgartner, I.: Gene and stem cell therapy in peripheral arterial occlusive disease. Vasc. Med. 13, 157–172 (2008)

    Google Scholar 

  35. Pacilli, A., Faggioli, G., Stella, A., Pasquinelli, G.: An update on therapeutic angiogenesis for peripheral vascular disease. Ann. Vasc. Surg. 24, 258–268 (2010)

    Google Scholar 

  36. Tateishi-Yuyama, E., Matsubara, H., Murohara, T., Ikeda, U., Shintani, S., Masaki, H., Amano, K., Kishimoto, Y., Yoshimoto, K., Akashi, H., Shimada, K., Iwasaka, T., Imaizumi, T.: Therapeutic Angiogenesis using Cell Transplantation Study I. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: A pilot study and a randomised controlled trial. Lancet 360, 427–435 (2002)

    Google Scholar 

  37. Esato, K., Hamano, K., Li, T.S., Furutani, A., Seyama, A., Takenaka, H., Zempo, N.: Neovascularization induced by autologous bone marrow cell implantation in peripheral arterial disease. Cell Transplantation 11, 747–752 (2002)

    Google Scholar 

  38. Miyamoto, K., Nishigami, K., Nagaya, N., Akutsu, K., Chiku, M., Kamei, M., Soma, T., Miyata, S., Higashi, M., Tanaka, R., Nakatani, T., Nonogi, H., Takeshita, S.: Unblinded pilot study of autologous transplantation of bone marrow mononuclear cells in patients with thromboangiitis obliterans. Circulation 114, 2679–2684 (2006)

    Google Scholar 

  39. Durdu, S., Akar, A.R., Arat, M., Sancak, T., Eren, N.T., Ozyurda, U.: Autologous bone-marrow mononuclear cell implantation for patients with rutherford grade ii-iii thromboangiitis obliterans. J. Vasc. Surg. 44, 732–739 (2006)

    Google Scholar 

  40. Murphy, M.P., Lawson, J.H., Rapp, B.M., Dalsing, M.C., Klein, J., Wilson, M.G., Hutchins, G.D., March, K.L.: Autologous bone marrow mononuclear cell therapy is safe and promotes amputation-free survival in patients with critical limb ischemia. J. Vasc. Surg. 53, 1565–1574 (2011). e1561

    Google Scholar 

  41. Patel, M.R., Conte, M.S., Cutlip, D.E., Dib, N., Geraghty, P., Gray, W., Hiatt, W.R., Ho, M., Ikeda, K., Ikeno, F., Jaff, M.R., Jones, W.S., Kawahara, M., Lookstein, R.A., Mehran, R., Misra, S., Norgren, L., Olin, J.W., Povsic, T.J., Rosenfield, K., Rundback, J., Shamoun, F., Tcheng, J., Tsai, T.T., Suzuki, Y., Vranckx, P., Wiechmann, B.N., White, C.J., Yokoi, H., Krucoff, M.W.: Evaluation and treatment of patients with lower extremity peripheral artery disease: Consensus definitions from peripheral academic research consortium (parc). J. Am. Coll. Cardiol. 65, 931–941 (2015)

    Google Scholar 

  42. Lu, D., Chen, B., Liang, Z., Deng, W., Jiang, Y., Li, S., Xu, J., Wu, Q., Zhang, Z., Xie, B., Chen, S.: Comparison of bone marrow mesenchymal stem cells with bone marrow-derived mononuclear cells for treatment of diabetic critical limb ischemia and foot ulcer: A double-blind, randomized, controlled trial. Diabetes Research And Clinical Practice 92, 26–36 (2011)

    Google Scholar 

  43. Bura, A., Planat-Benard, V., Bourin, P., Silvestre, J.S., Gross, F., Grolleau, J.L., Saint-Lebese, B., Peyrafitte, J.A., Fleury, S., Gadelorge, M., Taurand, M., Dupuis-Coronas, S., Leobon, B., Casteilla, L.: Phase i trial: The use of autologous cultured adipose-derived stroma/stem cells to treat patients with non-revascularizable critical limb ischemia. Cytotherapy 16, 245–257 (2014)

    Google Scholar 

  44. Marino, G., Moraci, M., Armenia, E., Orabona, C., Sergio, R., De Sena, G., Capuozzo, V., Barbarisi, M., Rosso, F., Giordano, G., Iovino, F., Barbarisi, A.: Therapy with autologous adipose-derived regenerative cells for the care of chronic ulcer of lower limbs in patients with peripheral arterial disease. The Journal of Surgical Research 185, 36–44 (2013)

    Google Scholar 

  45. Gupta, P.K., Chullikana, A., Parakh, R., Desai, S., Das, A., Gottipamula, S., Krishnamurthy, S., Anthony, N., Pherwani, A., Majumdar, A.S.: A double blind randomized placebo controlled phase i/ii study assessing the safety and efficacy of allogeneic bone marrow derived mesenchymal stem cell in critical limb ischemia. Journal of Translational Medicine 11, 143 (2013)

    Google Scholar 

  46. Walter, D.H., Krankenberg, H., Balzer, J.O., Kalka, C., Baumgartner, I., Schluter, M., Tonn, T., Seeger, F., Dimmeler, S., Lindhoff-Last, E., Zeiher, A.M., Investigators, P.: Intraarterial administration of bone marrow mononuclear cells in patients with critical limb ischemia: A randomized-start, placebo-controlled pilot trial (provasa). Circulation. Cardiovascular Interventions 4, 26–37 (2011)

    Google Scholar 

  47. Bartsch, T., Brehm, M., Zeus, T., Strauer, B.E.: Autologous mononuclear stem cell transplantation in patients with peripheral occlusive arterial disease. The Journal of Cardiovascular Nursing 21, 430–432 (2006)

    Google Scholar 

  48. Bartsch, T., Brehm, M., Zeus, T., Kogler, G., Wernet, P., Strauer, B.E.: Transplantation of autologous mononuclear bone marrow stem cells in patients with peripheral arterial disease (the tam-pad study). Clinical Research in Cardiology: Official Journal of the German Cardiac Society 96, 891–899 (2007)

    Google Scholar 

  49. Huang, P., Li, S., Han, M., Xiao, Z., Yang, R., Han, Z.C.: Autologous transplantation of granulocyte colony-stimulating factor-mobilized peripheral blood mononuclear cells improves critical limb ischemia in diabetes. Diabetes Care 28, 2155–2160 (2005)

    Google Scholar 

  50. Lenk, K., Adams, V., Lurz, P., Erbs, S., Linke, A., Gielen, S., Schmidt, A., Scheinert, D., Biamino, G., Emmrich, F., Schuler, G., Hambrecht, R.: Therapeutical potential of blood-derived progenitor cells in patients with peripheral arterial occlusive disease and critical limb ischaemia. European Heart Journal 26, 1903–1909 (2005)

    Google Scholar 

  51. Losordo, D.W., Kibbe, M.R., Mendelsohn, F., Marston, W., Driver, V.R., Sharafuddin, M., Teodorescu, V., Wiechmann, B.N., Thompson, C., Kraiss, L., Carman, T., Dohad, S., Huang, P., Junge, C.E., Story, K., Weistroffer, T., Thorne, T.M., Millay, M., Runyon, J.P., Schainfeld, R.: Autologous CDCTfCLII. A randomized, controlled pilot study of autologous cd34 + cell therapy for critical limb ischemia. Circulation Cardiovascular Interventions 5, 821–830 (2012)

    Google Scholar 

  52. Kinoshita, M., Fujita, Y., Katayama, M., Baba, R., Shibakawa, M., Yoshikawa, K., Katakami, N., Furukawa, Y., Tsukie, T., Nagano, T., Kurimoto, Y., Yamasaki, K., Handa, N., Okada, Y., Kuronaka, K., Nagata, Y., Matsubara, Y., Fukushima, M., Asahara, T., Kawamoto, A.: Long-term clinical outcome after intramuscular transplantation of granulocyte colony stimulating factor-mobilized cd34 positive cells in patients with critical limb ischemia. Atherosclerosis 224, 440–445 (2012)

    Google Scholar 

  53. Huang, P.P., Yang, X.F., Li, S.Z., Wen, J.C., Zhang, Y., Han, Z.C.: Randomised comparison of g-csf-mobilized peripheral blood mononuclear cells versus bone marrow-mononuclear cells for the treatment of patients with lower limb arteriosclerosis obliterans. Thrombosis and Haemostasis 98, 1335–1342 (2007)

    Google Scholar 

  54. Kawamoto, A., Katayama, M., Handa, N., Kinoshita, M., Takano, H., Horii, M., Sadamoto, K., Yokoyama, A., Yamanaka, T., Onodera, R., Kuroda, A., Baba, R., Kaneko, Y., Tsukie, T., Kurimoto, Y., Okada, Y., Kihara, Y., Morioka, S., Fukushima, M., Asahara, T.: Intramuscular transplantation of g-csf-mobilized cd34(+) cells in patients with critical limb ischemia: A phase i/iia, multicenter, single-blinded, dose-escalation clinical trial. Stem Cells 27, 2857–2864 (2009)

    Google Scholar 

  55. Mutirangura, P., Ruangsetakit, C., Wongwanit, C., Chinsakchai, K., Porat, Y., Belleli, A., Czeiger, D.: Enhancing limb salvage by non-mobilized peripheral blood angiogenic cell precursors therapy in patients with critical limb ischemia. Journal of the Medical Association of Thailand = Chotmaihet Thangphaet 92, 320–327 (2009)

    Google Scholar 

  56. Szabo, G.V., Kovesd, Z., Cserepes, J., Daroczy, J., Belkin, M., Acsady, G.: Peripheral blood-derived autologous stem cell therapy for the treatment of patients with late-stage peripheral artery disease-results of the short- and long-term follow-up. Cytotherapy 15, 1245–1252 (2013)

    Google Scholar 

  57. Ungerleider, J.L., Christman, K.L.: Concise review: Injectable biomaterials for the treatment of myocardial infarction and peripheral artery disease: Translational challenges and progress. Stem Cells Translational Medicine 3, 1090–1099 (2014)

    Google Scholar 

  58. Sun, H., Wang, X., Hu, X., Yu, W., You, C., Hu, H., Han, C.: Promotion of angiogenesis by sustained release of rhgm-csf from heparinized collagen/chitosan scaffolds. J. Biomed. Mater. Res. B Appl. Biomater. 100, 788–798 (2012)

    Google Scholar 

  59. Wee, S., Gombotz, W.R.: Protein release from alginate matrices. Adv. Drug Deliv. Rev. 31, 267–285 (1998)

    Google Scholar 

  60. Fischer, F.G., Dorfel, H.: [polyuronic acids in brown algae]. Hoppe-Seyler’s Zeitschrift fur physiologische Chemie 302, 186–203 (1955)

    Google Scholar 

  61. Haug, A.: Fractionation of alginic acid. Acta. Chem. Scand. 13, 601–613 (1959)

    Google Scholar 

  62. Lee, J., Lee, K.Y.: Local and sustained vascular endothelial growth factor delivery for angiogenesis using an injectable system. Pharmaceutical Research 26, 1739–1744 (2009)

    Google Scholar 

  63. Orive, G., Ponce, S., Hernandez, R.M., Gascon, A.R., Igartua, M., Pedraz, J.L.: Biocompatibility of microcapsules for cell immobilization elaborated with different type of alginates. Biomaterials 23, 3825–3831 (2002)

    Google Scholar 

  64. Crow, B.B., Nelson, K.D.: Release of bovine serum albumin from a hydrogel-cored biodegradable polymer fiber. Biopolymers 81, 419–427 (2006)

    Google Scholar 

  65. Eiselt, P., Lee, K.Y., Mooney, D.J.: Rigidity of two-component hydrogels prepared from alginate and poly(ethylene glycol)-diamines. Macromolecules 32, 5561–5566 (1999)

    Google Scholar 

  66. Smeds, K.A., Pfister-Serres, A., Miki, D., Dastgheib, K., Inoue, M., Hatchell, D.L., Grinstaff, M.W.: Photocrosslinkable polysaccharides for in situ hydrogel formation. Journal of Biomedical Materials Research 54, 115–121 (2001)

    Google Scholar 

  67. Zhao, S., Cao, M., Li, H., Li, L., Xu, W.: Synthesis and characterization of thermo-sensitive semi-ipn hydrogels based on poly(ethylene glycol)-co-poly(epsilon-caprolactone) macromer, n-isopropylacrylamide, and sodium alginate. Carbohydrate Research 345, 425–431 (2010)

    Google Scholar 

  68. Lee, K., Hong, H., Larson, R., Mooney, D.J.: Hydrogel formation via cell cross-linking. Advanced Materials 15, 1828–1832 (2003)

    Google Scholar 

  69. Friess, W.: Collagen- biomaterial for drug delivery. European Journal of Pharmaceutics and Bioppharmaceutics 45, 113–136 (1998)

    Google Scholar 

  70. Brinckmann, J., Notbohm, H., Muller, P.K.: Collagen: Primer in structure, processing and assembly. Springer-Verlag, Netherlands (2005)

    Google Scholar 

  71. Sinha, V.R., Trehan, A.: Biodegradable microspheres for protein delivery. Journal of Controlled Release 90, 261–280 (2003)

    Google Scholar 

  72. Cheng, W., Yan-hua, R., Fang-gang, N., Guo-an, Z.: The content and ration of type i and type iii collagen in skin differ with age and injury. African Journal of Biotechnology 10 (2011)

    Google Scholar 

  73. Harkness, R.D.: Collagen. Science Progress 54, 257–274 (1966)

    Google Scholar 

  74. He, L., Mu, C., Shi, J., Zhang, Q., Shi, B., Lin, W.: Modification of collagen with a natural cross-linker, procyanidin. International Journal of Biological Macromolecules 48, 354–359 (2011)

    Google Scholar 

  75. Gorham, S.D.: Collagen as a biomaterial. In: Byron, D. (ed.) Biomaterials, pp. 55–122. Stockton Press, New York (1991)

    Google Scholar 

  76. Gomez-Guillen, M.C., Perez-Mateos, M., Gomez-Estaca, J., Lopez-Caballero, E., Gimenez, B., Montero, P.: Fish gelatin: A renewable materials for developing active biodegradable films. Trends in Food Science & Technology 20, 3–16 (2009)

    Google Scholar 

  77. Zhang, F., Xu, S., Wang, Z.: Pre-treatment optimization and properties of gelatin from freshwater fish scales. Food and Bioproducts Processing (2010)

    Google Scholar 

  78. Gorgieva, S., Kokol, V.: Collagen- vs. Gelatine-based biomaterials and their biocompatibility: Review and perspectives. Interchopen (2011)

    Google Scholar 

  79. Netzel-Arnett, S., Mallya, S.K., Nagase, H., Birkedal-Hansen, H., Van Wart, H.E.: Continuously recording fluorescent assays optimized for five human matrix metalloproteinases. Analytical Biochemistry 195, 86–92 (1991)

    Google Scholar 

  80. Lynn, A.K., Yannas, L.V., Bonfield, W.: Antigenicity of immunogenicity of collagen. Journal of Biomedical Materials Research Part B: Applied Materials 71B, 343–354 (2004)

    Google Scholar 

  81. Olsen, D., Yang, C., Bodo, M., Chang, R., Leigh, S., Baez, J., Carmichael, D., Perala, M., Hamalainen, E.R., Jarvinen, M., Polarek, J.: Recombinant collagen and gelatin for drug delivery. Adv. Drug Deliv. Rev. 55, 1547–1567 (2003)

    Google Scholar 

  82. Hopkins, S.J., Wormall, A.: Pehyl isocyanate protein compounds and their immunological properties. Biophysical Journal 27, 740–753 (1933)

    Google Scholar 

  83. Starin, W.A.: The antigenic properties of gelain. The Journal of Infectious Diseases 23, 139–158 (1918)

    Google Scholar 

  84. Kokare, C.R.: Pharmaceutical microbiology- principles and applications, Pune, India (2008)

    Google Scholar 

  85. Taylor, P.M., Cass, A.E.G., Yacoub, M.H.: Extracellular matrix scaffolds for tissue engineering heart valves. Process in Pediatric Cardiology 21, 219–225 (2006)

    Google Scholar 

  86. Sisson, K., Zhang, C., Farach-Carson, M.C., Chase, D.B., Rabolt, J.F.: Evaluation of cross-linking methods for electrospun gelatin on cell growth and viability. Biomacromolecules 10, 1675–1680 (2009)

    Google Scholar 

  87. Yannas, I.V.: Tissue regeneration by use of collagen-glycosaminoglycan co-polymers. Clinical Materials 9, 179–184 (1992)

    Google Scholar 

  88. Tefft, S., Bentz, J., Estridge, T.D.: Collagen and heparin matrices for growth factor delivery. Journal of Controlled Release 48, 29–33 (1997)

    Google Scholar 

  89. Mohanty, B., Bohidar, H.B.: Systematic of alcohol-induced simple coacervation in aqueous gelatin solutions. Biomacromolecules 4, 1080–1086 (2003)

    Google Scholar 

  90. Mohanty, B., Bohidar, H.B.: Microscopic structure of gelatin coacervates. International Journal of Biological Macromolecules 36, 39–46 (2005)

    Google Scholar 

  91. Drury, J.L., Mooney, D.J.: Hydrogels for tissue engineering: Scaffold design variables and applications. Biomaterials 24, 4337–4351 (2003)

    Google Scholar 

  92. Lee, K.Y., Mooney, D.J.: Hydrogels for tissue engineering. Chemical Reviews 101, 1869–1879 (2001)

    Google Scholar 

  93. Kloxin, A.M., Kasko, A.M., Salinas, C.N., Anseth, K.S.: Photodegradable hydrogels for dynamic tuning of physical and chemical properties. Science 324, 59–63 (2009)

    Google Scholar 

  94. Hern, D.L., Hubbell, J.A.: Incorporation of adhesion peptides into nonadhesive hydrogels useful for tissue resurfacing. Journal of Biomedical Materials Research 39, 266–276 (1998)

    Google Scholar 

  95. Huebsch, N., Arany, P.R., Mao, A.S., Shvartsman, D., Ali, O.A., Bencherif, S.A., Rivera-Feliciano, J., Mooney, D.J.: Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nature Materials 9, 518–526 (2010)

    Google Scholar 

  96. Sundararaghavan, H.G., Burdick, J.A.: Gradients with depth in electrospun fibrous scaffolds for directed cell behavior. Biomacromolecules 12, 2344–2350 (2011)

    Google Scholar 

  97. Sukarto, A., Yu, C., Flynn, L.E., Amsden, B.G.: Co-delivery of adipose-derived stem cells and growth factor-loaded microspheres in rgd-grafted n-methacrylate glycol chitosan gels for focal chondral repair. Biomacromolecules 13, 2490–2502 (2012)

    Google Scholar 

  98. Kim, J.K., Kim, H.J., Chung, J.Y., Lee, J.H., Young, S.B., Kim, Y.H.: Natural and synthetic biomaterials for controlled drug delivery. Archives of Pharmacal Research 37, 60–68 (2014)

    Google Scholar 

  99. Keys, K., Andreopoulos, F.M., Peppas, N.A.: Poly(ethylene glycol) star polymer hydrogels. Macromolecules 31, 8149–8156 (1998)

    Google Scholar 

  100. Liu, V.A., Bhatia, S.N.: Three-dimensional photopatterning of hydrogels containing living cells. Biomedical Devices 4, 257–266 (2002)

    Google Scholar 

  101. Chan, V., Zorlutuna, P., Jeong, J.H., Kong, H., Bashir, R.: Three-dimensional photopatterning of hydrogels using stereolithography for long-term cell encapsulation. Lab on a Chip 10, 2062–2070 (2010)

    Google Scholar 

  102. Kade, M., Burke, D.J., Hawker, C.: The power of thiol-ene chemistry. Journal of Polymer Science Part A 48, 743–750 (2010)

    Google Scholar 

  103. Park, K.H., Na, K., Kim, S.W., Jung, S.Y., Park, K.H., Chung, H.M.: Phenotype of hepatocyte spheroids behavior within thermo-sensitive poly(nipaam-co-peg-g-grgds) hydrogel as a cell delivery vehicle. Biotechnology Letters 27, 1081–1086 (2005)

    Google Scholar 

  104. Jeong, B., Bae, Y.H., Kim, S.W.: Drug release from biodegradable injectable thermosensitive hydrogel of peg–plga–peg triblock copolymers. Journal of Controlled Release 63, 155–163 (2000)

    Google Scholar 

  105. Jeong, J.H., Chan, V., Cha, C., Zorlutuna, P., Dyck, C., Hsia, K.J., Bashir, R., Kong, H.: “Living” microvascular stamp for patterning of functional neovessels; orchestrated control of matrix property and geometry. Adv. Mater. 24(58–63), 51 (2012)

    Google Scholar 

  106. Peyton, S.R., Raub, C.B., Keschrumrus, V.P., Putnam, A.J.: The use of poly(ethylene glycol) hydrogels to investigate the impact of ecm chemistry and mechanics on smooth muscle cells. Biomaterials 27, 4881–4893 (2006)

    Google Scholar 

  107. Kong, H.J., Boontheekul, T., Mooney, D.J.: Quantifying the relation between adhesion ligand-receptor bond formation and cell phenotype. Proc. Natl. Acad. Sci. USA 103, 18534–18539 (2006)

    Google Scholar 

  108. Kong, H.J., Hsiong, S., Mooney, D.J.: Nanoscale cell adhesion ligand presentation regulates nonviral gene delivery and expression. Nano Letters 7, 161–166 (2007)

    Google Scholar 

  109. Rizzi, S.C., Hubbell, J.A.: Recombinant protein-co-peg networks as cell-adhesive and proteolytically degradable hydrogel matrixes. Part i: Development and physicochemical characteristics. Biomacromolecules 6, 1226–1238 (2005)

    Google Scholar 

  110. Layman, H., Sacasa, M., Murphy, A.E., Murphy, A.M., Pham, S.M., Andreopoulos, F.M.: Co-delivery of fgf-2 and g-csf from gelatin-based hydrogels as angiogenic therapy in a murine critical limb ischemic model. Acta Biomaterialia 5, 230–239 (2009)

    Google Scholar 

  111. Ruvinov, E., Leor, J., Cohen, S.: The effects of controlled hgf delivery from an affinity-binding alginate biomaterial on angiogenesis and blood perfusion in a hindlimb ischemia model. Biomaterials 31, 4573–4582 (2010)

    Google Scholar 

  112. Anderson, E.M., Kwee, B.J., Lewin, S.A., Raimondo, T., Mehta, M., Mooney, D.J.: Local delivery of vegf and sdf enhances endothelial progenitor cell recruitment and resultant recovery from ischemia. Tissue engineering. Part A (2014)

    Google Scholar 

  113. Phelps, E.A., Landázuri, N., Thulé, P.M., Taylor, W.R., García, A.J.: Bioartificial matrices for therapeutic vascularization. Proceedings of the National Academy of Sciences 107, 3323–3328 (2010)

    Google Scholar 

  114. Zachman, A.L., Wang, X., Tucker-Schwartz, J.M., Fitzpatrick, S.T., Lee, S.H., Guelcher, S.A., Skala, M.C., Sung, H.-J.: Uncoupling angiogenesis and inflammation in peripheral artery disease with therapeutic peptide-loaded microgels. Biomaterials 35, 9635–9648 (2014)

    Google Scholar 

  115. Kim, J.H., Jung, Y., Kim, B.-S., Kim, S.H.: Stem cell recruitment and angiogenesis of neuropeptide substance p coupled with self-assembling peptide nanofiber in a mouse hind limb ischemia model. Biomaterials 34, 1657–1668 (2013)

    Google Scholar 

  116. Poole, K.M., Nelson, C.E., Joshi, R.V., Martin, J.R., Gupta, M.K., Haws, S.C., Kavanaugh, T.E., Skala, M.C., Duvall, C.L.: Ros-responsive microspheres for on demand antioxidant therapy in a model of diabetic peripheral arterial disease. Biomaterials 41, 166–175 (2015)

    Google Scholar 

  117. Domanchuk, K., Ferrucci, L., Guralnik, J.M., Criqui, M.H., Tian, L., Liu, K., Losordo, D., Stein, J., Green, D., Kibbe, M., Zhao, L., Annex, B., Perlman, H., Lloyd-Jones, D., Pearce, W., Taylor, D., McDermott, M.M.: Progenitor cell release plus exercise to improve functional performance in peripheral artery disease: The propel study. Contemporary Clinical Trials 36, 502–509 (2013)

    Google Scholar 

  118. Schwarz, T.M., Leicht, S.F., Radic, T., Rodriguez-Araboalaza, I., Hermann, P.C., Berger, F., Saif, J., Böcker, W., Ellwart, J.W., Aicher, A.: Vascular incorporation of endothelial colony-forming cells is essential for functional recovery of murine ischemic tissue following cell therapy. Arteriosclerosis, Thrombosis, And Vascular Biology 32, e13–e21 (2012)

    Google Scholar 

  119. Katare, R., Stroemer, P., Hicks, C., Stevanato, L., Patel, S., Corteling, R., Miljan, E., Vishnubhatla, I., Sinden, J., Madeddu, P.: Clinical-grade human neural stem cells promote reparative neovascularization in mouse models of hindlimb ischemia. Arteriosclerosis, Thrombosis, And Vascular Biology 34, 408–418 (2014)

    Google Scholar 

  120. Kim, D.W., Jun, I., Lee, T.-J., hye Lee, J., Lee, Y.J., Jang, H.-K., Kang, S., Park, K.D., Cho, S.-W., Kim, B.-S.: Therapeutic angiogenesis by a myoblast layer harvested by tissue transfer printing from cell-adhesive, thermosensitive hydrogels. Biomaterials 34, 8258–8268 (2013)

    Google Scholar 

  121. Chen, D.-Y., Wei, H.-J., Lin, K.-J., Huang, C.-C., Wang, C.-C., Wu, C.-T., Chao, K.-T., Chen, K.-J., Chang, Y., Sung, H.-W.: Three-dimensional cell aggregates composed of huvecs and cbmscs for therapeutic neovascularization in a mouse model of hindlimb ischemia. Biomaterials 34, 1995–2004 (2013)

    Google Scholar 

  122. Landazuri, N., Levit, R.D., Joseph, G., Ortega-Legaspi, J.M., Flores, C.A., Weiss, D., Sambanis, A., Weber, C.J., Safley, S.A., Taylor, W.R.: Alginate microencapsulation of human mesenchymal stem cells as a strategy to enhance paracrine-mediated vascular recovery after hindlimb ischaemia. Journal of Tissue Engineering And Regenerative Medicine (2012)

    Google Scholar 

  123. Rufaihah, A.J., Huang, N.F., Jamé, S., Lee, J.C., Nguyen, H.N., Byers, B., De, A., Okogbaa, J., Rollins, M., Reijo-Pera, R.: Endothelial cells derived from human ipscs increase capillary density and improve perfusion in a mouse model of peripheral arterial disease. Arteriosclerosis, Thrombosis And Vascular Biology 31, e72–e79 (2011)

    Google Scholar 

  124. Mulyasasmita, W., Cai, L., Dewi, R.E., Jha, A., Ullmann, S.D., Luong, R.H., Huang, N.F., Heilshorn, S.C.: Avidity-controlled hydrogels for injectable co-delivery of induced pluripotent stem cell-derived endothelial cells and growth factors. Journal of Controlled Release : Official Journal of the Controlled Release Society 191, 71–81 (2014)

    Google Scholar 

  125. Grochot-Przeczek, A., Dulak, J., Jozkowicz, A.: Therapeutic angiogenesis for revascularization in peripheral artery disease. Gene 525, 220–228 (2013)

    Google Scholar 

  126. Sedighiani, F., Nikol, S.: Gene therapy in vascular disease. Surgeon 9, 326–335 (2011)

    Google Scholar 

  127. Khan, T.A., Sellke, F.W., Laham, R.J.: Gene therapy progress and prospects: Therapeutic angiogenesis for limb and myocardial ischemia. Gene Ther. 10, 285–291 (2003)

    Google Scholar 

  128. Yang, F., Cho, S.-W., Son, S.M., Bogatyrev, S.R., Singh, D., Green, J.J., Mei, Y., Park, S., Bhang, S.H., Kim, B.-S.: Genetic engineering of human stem cells for enhanced angiogenesis using biodegradable polymeric nanoparticles. Proceedings of the National Academy of Sciences 107, 3317–3322 (2010)

    Google Scholar 

  129. Katare, R., Riu, F., Rowlinson, J., Lewis, A., Holden, R., Meloni, M., Reni, C., Wallrapp, C., Emanueli, C., Madeddu, P.: Perivascular delivery of encapsulated mesenchymal stem cells improves postischemic angiogenesis via paracrine activation of vegf-a. Arteriosclerosis, Thrombosis And Vascular Biology 33, 1872–1880 (2013)

    Google Scholar 

  130. Jazwa, A., Stepniewski, J., Zamykal, M., Jagodzinska, J., Meloni, M., Emanueli, C., Jozkowicz, A., Dulak, J.: Pre-emptive hypoxia-regulated ho-1 gene therapy improves post-ischaemic limb perfusion and tissue regeneration in mice. Cardiovascular Research 97, 115–124 (2013)

    Google Scholar 

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Balikov, D.A., Lee, S.H., Boire, T.C., Lee, Jb., Zachman, A.L., Sung, HJ. (2016). Engineering Integrative Stem Cell and Biomaterial Therapies for Peripheral Artery Disease. In: Jo, H., Jun, HW., Shin, J., Lee, S. (eds) Biomedical Engineering: Frontier Research and Converging Technologies. Biosystems & Biorobotics, vol 9. Springer, Cham. https://doi.org/10.1007/978-3-319-21813-7_6

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