Chitosan stabilizes platelet growth factors and modulates stem cell differentiation toward tissue regeneration

Carbohydrate Polymers

Volumn 98, Issue 1, 2013, Pages 665-676

  Busilacchi, Alberto ^a   Gigante, Antonio ^a   Mattioli Belmonte, Monica ^a   Manzotti, Sandra ^a   Muzzarelli, Riccardo A A ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

Chitosan; Growth factors; Platelets; Stem cells; Tissue regeneration; Wound healing

Indexed keywords

BIOMATERIALS; BONE; CELL CULTURE; CELLS; CHITIN; CHITOSAN; CYTOLOGY; HISTOLOGY; NANOCOMPOSITES; PLATELETS; STEM CELLS; TISSUE;

ADIPOSE DERIVED STEM CELLS; BIOCHEMICAL CHARACTERISTICS; GROWTH FACTOR; MESENCHYMAL STEM CELL; OSTEOGENIC DIFFERENTIATION; STEM CELL DIFFERENTIATION; TRI-CALCIUM PHOSPHATES; WOUND HEALING;

TISSUE REGENERATION;

ALKALINE PHOSPHATASE; ALP; BONE MORPHOGENETIC PROTEIN; CHITOSAN; FIBROBLAST GROWTH FACTOR; GLYCOSAMINOGLYCAN; GREEN FLUORESCENT PROTEIN; PLATELET DERIVED GROWTH FACTOR; SIGNAL PEPTIDE; SOMATOMEDIN; SUPEROXIDE DISMUTASE; VASCULOTROPIN;

ADIPOSE DERIVED STEM CELL; ADSC; AFM; ANIMAL; ARG-GLY-ASP TRIPEPTIDE; ATOMIC FORCE MICROSCOPY; BMP; BMSC; BONE MARROW STEM CELLS; CA(3)P(2)O(8); CELL DIFFERENTIATION; CYTOLOGY; DMEM; DRUG EFFECT; DULBECCO MODIFIED EAGLE'S MEDIUM; ECM; EMBRYONIC STEM CELL; ESC; EXTRACELLULAR MATRIX; FGF; GAG; GF; GFP; GROWTH FACTORS; H&E; HEMATOPOIETIC PROGENITOR CELLS; HEMATOPOIETIC STEM CELL; HEMATOXYLIN AND EOSIN; HPC; HSC; HUMAN; IGF; MESENCHYMAL STEM CELL; METABOLISM; METHODOLOGY; MSC; N-METHYLIMIDAZOLE CHITOSAN; NMI-CHITOSAN; PDLSC; PERIODONTAL LIGAMENT STEM CELLS; PLATELETS; PRP; REVIEW; RGD; SA-CHITOSAN; SALICYLATE-MODIFIED CHITOSAN; SOD; STEM CELL; TGF-Β; THROMBOCYTE; THROMBOCYTE RICH PLASMA; THROMBOXANE A(2); TISSUE REGENERATION; TRANSFORMING GROWTH FACTOR-Β; TRICALCIUM ORTHOPHOSPHATE; TXA(2); WOUND HEALING;

ADIPOSE DERIVED STEM CELL; ADSC; AFM; ALKALINE PHOSPHATASE; ALP; ARG-GLY-ASP TRIPEPTIDE; ATOMIC FORCE MICROSCOPY; BMP; BMSC; BONE MARROW STEM CELLS; BONE MORPHOGENETIC PROTEIN; CA(3)P(2)O(8); CHITOSAN; DMEM; DULBECCO MODIFIED EAGLE'S MEDIUM; ECM; EMBRYONIC STEM CELLS; ESC; EXTRACELLULAR MATRIX; FGF; FIBROBLAST GROWTH FACTOR; GAG; GF; GFP; GLYCOSAMINOGLYCANS; GREEN FLUORESCENT PROTEIN; GROWTH FACTORS; H&E; HEMATOPOIETIC PROGENITOR CELLS; HEMATOPOIETIC STEM CELLS; HEMATOXYLIN AND EOSIN; HPC; HSC; IGF; INSULIN-LIKE GROWTH FACTOR; MESENCHYMAL STEM CELL; MSC; N-METHYLIMIDAZOLE CHITOSAN; NMI-CHITOSAN; PDGF; PDLSC; PERIODONTAL LIGAMENT STEM CELLS; PLATELET DERIVED GROWTH FACTOR; PLATELET-RICH PLASMA; PLATELETS; PRP; RGD; SA-CHITOSAN; SALICYLATE-MODIFIED CHITOSAN; SOD; STEM CELLS; SUPEROXIDE DISMUTASE; TGF-Β; THROMBOXANE A(2); TISSUE REGENERATION; TRANSFORMING GROWTH FACTOR-Β; TRICALCIUM ORTHOPHOSPHATE; TXA(2); VASCULAR ENDOTHELIAL GROWTH FACTOR; VEGF; WOUND HEALING;

ANIMALS; BLOOD PLATELETS; CELL DIFFERENTIATION; CHITOSAN; GUIDED TISSUE REGENERATION; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; STEM CELLS;

EID: 84884593350     PISSN: 01448617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.carbpol.2013.06.044     Document Type: Review

References (137)

1. Aghaloo, T. L., Moy, P. K., & Freymiller, E. G. (2002). Investigation of platelet-rich plasma in rabbit cranial defects: A pilot study. Journal of Oral and Maxillofacial Surgery, 60, 1176-1181.
2. Ahtee, L., Boullin, D. J., & Passonen, M. K. (1974). Transport of taurine by normal human blood platelets. British Journal of Pharmacy, 52, 245-251.
3. Alemdaroglu, C., Degim, Z., Celebi, N., Zor, F., Ozturk, S., & Erdogan, D. (2006). An investigation on burn wound healing in rats with chitosan gel formulation containing epidermal growth factor. Burns, 32, 319-327.
4. Altman, A. M., Yan, Y. S., Matthias, N., Bai, X. W., Rios, C., Mathur, A. B., et al. (2009). Ifats collection: Human adipose-derived stem cells seeded on a silk fibroin-chitosan scaffold enhance wound repair in a murine soft tissue injury model. Stem Cells, 27, 250-258.
5. Bai, M. Y., Chou, T. C., Tsai, J. C., & Yang, H. C. (2013). Active ingredient-containing chitosan/ polycaprolactone nonwoven mats: Characterizations and their functional assays. Materials Science & Engineering C, 33, 224-233.
6. Basaran, E., & Yazan, Y. (2012). Ocular application of chitosan. Expert Opinion on Drug Delivery, 9, 701-712.
7. Bi, L., Cheng, W., Fan, H., & Pei, G. (2010). Reconstruction of goat tibial defects using an injectable tricalcium phosphate/chitosan in combination with autologous platelet-rich plasma. Biomaterials, 31, 3201-3211.
8. Borzini, P., & Mazzucco, L. (2005). Platelet gels and releasates. Current Opinions in Hematology, 12, 473-479. (Pubitemid 41546479)
9. Bourque, W. T., Gross, M., & Hall, B. K. (1993). Expression of four growth factors during fracture repair. International Journal of Development Biology, 37, 573-579. (Pubitemid 24063759)
10. Calori, G. M., Tagliabue, L., Gala, L., d'Imporzano, M., Peretti, G., & Albisetti, W. (2008). Application of rhBMP-7 and platelet-rich plasma in the treatment of long bone non-unions: A prospective randomised clinical study on 120 patients. Injury, 39, 1391-1402.
11. Carter, M. J., Fylling, C. P., Li, W. W., de Leon, J., Driver, V. R., Serena, T. E., et al. (2011). Analysis of run-in and treatment data in a wound outcomes registry: Clinical impact of topical platelet-rich plasma gel on healing trajectory. International Wound Journal, 8, 638-650.
12. Centeno, C. J., Busse, D., Kisiday, J., Keohan, C., & Freeman, M. (2008). Increased knee cartilage volume in degenerative joint disease using percutaneously implanted autologous mesenchymal stem cells platelet lysate and dexamethasone. American Journal of Case Reports, 9, 246-251.
13. Chang, C., Peng, N., He, M., Teramoto, Y., Nishio, Y., & Zhang, L. (2013). Fabrication and properties of chitin/hydroxyapatite hybrid hydrogels as scaffold nano-materials. Carbohydrate Polymers, 91, 7-13.
14. Chen, W. C., Zhou, H. Z., Weir, M. D., Tang, M. H., Bao, C. Y., & Xu, H. H. K. (2013). Human embryonic stem cell-derived mesenchymal stem cell seeding on calcium phosphate cement-chitosan-RGD scaffold for bone repair. Tissue Engineering A, 19, 915-927.
15. Coller, B. S. (1984). Bizzozero and the discovery of the blood platelets. Lancet, 804-806.
16. Croisier, F., & Jerome, C. (2013). Chitosan-based biomaterials for tissue engineering. European Polymer Journal, 49, 780-792.
17. Crovetti, G., Martinelli, G., & Issi, M. (2004). Platelet gel for healing cutaneous chronic wounds. Transfusion and Apheresis Sciences, 30, 145-151. (Pubitemid 38519799)
18. Daley, W. P., Peters, S. B., & Larsen, M. (2008). Extracellular matrix dynamics in development and regeneration medicine. Journal of Cell Science, 121, 255-264. (Pubitemid 351356696)
19. De Angelis, B., Lucarini, L., Orlandi, F., Agovino, A., Migner, A., Cervelli, V., et al. (2012). Regenerative surgery of the complications with Morton's neuroma surgery: Use of platelet rich plasma and hyaluronic acid. International Wound Journal, http://dx.doi.org/10.1111/j.1742-481X.2012.00992.x
20. Debnath, T., Chelluri, L. K., Beevi, S. S., Verma, V., Shalini, P. U., Lakshmi, K., et al. (2013). An approach towards the proliferation and differentiation of stem cells on chitosan based soluble polymer. Cytotherapy, 15, S43.
21. Degim, Z. (2008). Use of microparticulate systems to accelerate skin wound healing. Journal of Drug Targeting, 16, 437-448. (Pubitemid 352015812)
22. Degim, Z., Celebi, N., Alemdaroglu, C., Deveci, M., Ozturk, S., & Ozogul, C. (2011). Evaluation of chitosan gel containing liposome-loaded epidermal growth factor on burn wound healing. International Wound Journal, 8, 343-354.
23. Degim, Z., Celebi, N., Sayan, H., Babul, A., Erdogan, D., & Take, G. (2002). An investigation on skin wound healing in mice with a taurine-chitosan gel formulation. Amino Acids, 22, 187-198. (Pubitemid 34253358)
24. Devlin, J. J., Kircher, S., Kozen, B. G., Littlejohn, L. F., & Johnson, A. S. (2011). Comparison of ChitoFlex® Celox® and QuikClot® in control of hemorrhage. The Journal of Emergency Medicine, 41, 237-245.
25. Ding, K., Zhang, Y. L., Yang, Z., & Xu, J. Z. (2013). A promising injectable scaffold: The biocompatibility and effect on osteogenic differentiation of mesenchymal stem cells. Biotechnology and Bioprocess Engineering, 18, 155-163.
26. Dionyssiou, D., Demiri, E., Foroglou, P., Cheva, A., Saratzis, N., Aivazidis, C., et al. (2012). The effectiveness of intralesional injection of platelet-rich plasma in accelerating the healing of chronic ulcers. An experimental and clinical study. International Wound Journal, http://dx.doi.org/10.1111/j.1742-481X.2012.00996.x
27. Dong, J., Uemura, T., Shirasaki, Y., & Tateishi, T. (2002). Promotion of bone formation using highly pure porous beta-TCP combined with bone marrow-derived osteoprogenitor cells. Biomaterials, 23, 4493-4502. (Pubitemid 36151601)
28. Dyondi, D., Chandra, V., Bhonde, R. R., & Banerjee, R. (2012). Development and characterization of dual growth factor loaded in situ gelling biopolymeric system for tissue engineering applications. Journal of Biomaterials and Tissue Engineering, 2, 67-75.
29. Ehrenfest, D. M., Rasmusson, L. T., & Albrektsson, T. (2009). Classification of platelet concentrates: From pure platelet-rich plasma to leucocyte- and platelet-rich fibrin. Trends in Biotechnology, 27, 158-167.
30. Fischer, T. H., Bode, A. P., Demcheva, M., & Vournakis, J. N. (2007). Hemostatic properties of glucosamine-based materials. Journal of Biomedical Materials Research, 80A, 167-174. (Pubitemid 44913344)
31. Fischer, T. H., Thatte, H. S., Nichols, T. C., Bender-Neal, D. E., Bellinger, D. A., & Vournakis, J. N. (2005). Synergistic platelet integrin signaling and factor XII activation in poly-N-acetyl glucosamine fiber-mediated hemostasis. Biomaterials, 26, 5433-5443. (Pubitemid 40592133)
32. Frendo, J., Koj, A., & Zgliczynski, J. M. (1959). Taurine in human blood platelets. Nature, 183, 685-686.
33. Gao, C., Cai, Y. R., Kong, X. D., Han, G. X., & Yao, J. M. (2013). Development and characterization of injectable chitosan-based hydrogels containing dexamethasone/rhBMP-2 loaded hydroxyapatite nanoparticles. Materials Letters, 93, 312-315.
34. Ge, S. H., Zhao, N., Wang, L., Yu, M. J., Liu, H., Song, A. M., et al. (2012). Bone repair by periodontal ligament stem cell-seeded nanohydroxyapatite-chitosan scaffold. International Journal of Nanomedicine, 7, 5405-5414.
35. Geremicca, W., Fonte, C., & Vecchio, S. (2010). Blood components for topical use in tissue regeneration: Evaluation of corneal lesions treated with platelet lysate and considerations on repair mechanisms. Blood Transfusion, 8, 107-112.
36. Gigante, A., Cappella, M., Manzotti, S., Cecconi, S., Greco, F., Primio, R. D. I., et al. (2010). Osteoinduction properties of different growth factors on cells from non-union patients: In vitro study for clinical application. Journal of Biological Regulators and Homeostatic Agents, 24, 51-62.
37. Gigante, A., Del Torto, M., Manzotti, S., Cianforlini, M., Busilacchi, A., Davidson, P. A., et al. (2012). Platelet rich fibrin matrix effects on skeletal muscle lesions: An experimental study. Journal of Biological Regulators and Homeostatic Agents, 26, 475-484.
38. Gimble, J. M., Katz, A. J., & Bunnell, B. A. (2007). Adipose-derived stem cells for regenerative medicine. Circulation Research, 100, 1249-1260. (Pubitemid 46742916)
39. Gjelstrup, L., & Stelzer, T. (2012). Expansion and differentiation of human mesenchymal stromal cells. VWR bioMarke, 28, 20-22.
40. Gollehon, T. J., King, D. E., & Craig, F. E. (1998). Does hyperconcentration result in platelet activation? A flow-cytometric study of hyperconcentrated random donor platelets. Vox Sanguinis, 75, 124-127. (Pubitemid 28490882)
41. Gravela, E. (1989). Giulio Bizzozero. Torino, Italy: Allemandi C.
42. Griffin, X. L., Smith, C. M., & Costa, M. L. (2009). The clinical use of platelet-rich plasma in the promotion of bone healing: A systematic review. Injury, 40, 158-162.
43. Han, J., Meng, H. X., Tang, J. M., Li, S. L., Tang, Y., & Chen, Z. B. (2007). The effect of different platelet-rich plasma concentrations on proliferation and differentiation of human periodontal ligament cells in vitro. Cell Proliferation, 40, 241-252. (Pubitemid 46398819)
44. Hanna, J. H., Saha, K., & Jaenisch, R. (2010). Pluripotency and cellular reprogramming: Facts, hypotheses, unresolved issues. Cell, 143, 508-525.
45. Haque, A., Yue, X. S., Motazedian, A., Tagawa, Y., & Akaike, T. (2012). Characterization and neural differentiation of mouse embryonic and induced pluripotent stem cells on cadherin-based substrata. Biomaterials, 33, 5094-5106.
46. Hayashi, Y., Yamada, S., Guchi, K. Y., Koyama, Z., & Ikeda, T. (2012). Chitosan and fish collagen as biomaterials for regenerative medicine. Advances in Food and Nutrition Research, 65, 107-120.
47. Hunter, K. T., & Ma, T. (2013). In vitro evaluation of hydroxyapatite chitosan gelatin composite membrane in guided tissue regeneration. Journal of Biomedical Materials Research, 101A, 1016-1025.
48. Huxtable, R. J., Azuma, J., Kuriyama, K., Nakagawa, M., & Baba, A. (Eds.). (1996). Taurine basic and clinical aspects. (pp. 589-595). New York: Plenum Press.
49. Iacono, E., Merlo, B., Pirrone, A., Antonelli, C., Brunori, L., Romagnoli, N., et al. (2012). Effects of mesenchymal stem cells isolated from amniotic fluid and plateletrich plasma gel on severe decubitus ulcers in a septic neonatal foal. Research Veterinary Science, 93, 1439-1440.
50. Jaenisch, R., & Young, R. (2008). Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell, 132, 567-582. (Pubitemid 351253686)
51. Jain, A., Gulbake, A., Shilpi, S., Jain, A., Hurkat, P., & Jain, S. K. (2013). A new horizon in modifications of chitosan: Syntheses and applications. Critical Reviews in Therapeutic Drug Carrier Systems, 30, 91-181.
52. Jiang, T., Deng, M., Abdel-Fattah, W. I., & Laurencin, C. T. (2012). Chitosan-based biopharmaceutical scaffolds in tissue engineering and regenerative medicine. In B. Sarmento, & J. DasNeves (Eds.), Chitosan-based systems for biopharmaceuticals (pp. 393-427). Chichester: Wiley.
53. Judith, R., Nithya, M., Rose, C., & Mandal, A. B. (2010). Application of a PDGFcontaining novel gel for cutaneous wound healing. Life Sciences, 87, 1-8.
54. Judith, R., Nithya, M., Rose, C., & Mandal, A. B. (2012). Biopolymer gel matrix as acellular scaffold for enhanced dermal tissue regeneration. Biologicals, 40, 231-239.
55. Kanczler, J. M., & Oreffo, R. O. (2008). Osteogenesis and angiogenesis: The potential for engineering bone. European Cell Materials, 15, 100-114. (Pubitemid 351955734)
56. Kaully, T., Kaufman-Francis, K., Lesman, A., & Levenberg, S. (2009). Vascularization: The conduit to viable engineered tissues. Tissue Engineering Part B Reviews, 15, 159-169.
57. Kellouche, S., Martin, C., Korb, G., Rezzonico, R., Bouard, D., Benbunan, M., et al. (2007). Tissue engineering for full-thickness burns: A dermal substitute from bench to bedside. Biochemical and Biophysical Research Communications, 363, 472-478. (Pubitemid 47520679)
58. Kim, J. A., Ahn, B. N., Kong, C. S., & Kim, S. K. (2012). Chitooligomers inhibit UVA- induced photoaging of skin by regulating TGF-beta/Smad signaling cascade. Carbohydrate Polymers, 88, 490-495.
59. Klokkevold, P. R., Fukayama, H., Sung, E. C., & Bertolami, C. N. (1999). The effect of chitosan poly(N-acetyl glucosamine) on lingual hemostasis in heparinized rabbits. Journal of Oral and Maxillofacial Surgery, 57, 49-52. (Pubitemid 29024875)
60. Kuo, Y. C., & Lin, C. C. (2013). Accelerated nerve regeneration using induced pluripotent stem cells in chitin-chitosan-gelatin scaffolds with inverted colloidal crystal geometry. Colloids and Surfaces B, 103, 595-600.
61. Kuo, Y. C., & Wang, C. C. (2013). Guided differentiation of induced pluripotent stem cells into neuronal lineage in alginate-chitosan-gelatin hydogels with surface neuron growth factor. Colloids and Surfaces B, 103, 194-199.
62. Kutlu, B., Aydin, R. S. T., Akman, A. C., Gumusderelioglu, M., & Nohutcu, R. M. (2013). Platelet-rich plasma-loaded chitosan scaffolds: Preparation and growth factor release kinetics. Journal of Biomedical Materials Research, 101B, 28-35.
63. Lee, Y. M., Park, Y. J., Lee, S. J., Ku, Y., Han, S. B., Klokkevold, P. R., et al. (2000). The bone regenerative effect of platelet-derived growth factor-BB delivered with a chitosan/tricalcium phosphate sponge carrier. Journal of Periodontology, 71, 418-424.
64. Leytin, V., Mody, M., Semple, J. W., Garvey, B., & Freedman, J. (2000). Flow cytometric parameters for characterizing platelet activation by measuring P-selectin (CD62) expression: Theoretical consideration and evaluation in thrombintreated platelet populations. Biochemical Biophysical Research Communications, 269, 85-90. (Pubitemid 30440259)
65. Liu, X., Ma, L., Mao, Z. W., & Gao, C. Y. (2011). Chitosan-based biomaterials for tissue repair and regeneration. In R. Jayakumar, M. Prabaharan, & R. A. A. Muzzarelli (Eds.), Chitosan for Biomaterials, Advances in Polymer Science (244) (pp. 81-128). Berlin: Springer.
66. Lieberman, J. R., Daluiski, A., & Einhorn, T. A. (2002). The role of growth factors in the repair of bone: Biology and clinical applications. Journal of Bone Joint Surgery, 84A, 1032-1044.
67. Lord, M. S., Cheng, B., McCarthy, S. J., Jung, M., & Whitelock, J. M. (2011). The modulation of platelet adhesion and activation by chitosan through plasma and extracellular matrix proteins. Biomaterials, 32, 6655-6662.
68. Maciel, F. B., DeRossi, R., Modolo, T. J. C., Pagliosa, R. C., Leal, C. R. J., & Delben, A. A. S. T. (2012). Scanning electron microscopy and microbiological evaluation of equine burn wound repair after platelet-rich plasma gel treatment. Burns, 38, 1058-1065.
69. Man, Y., Wang, P., Guo, Y., Xiang, L., Yang, Y., Qu, Y., et al. (2012). Angiogenic and osteogenic potential of platelet-rich plasma and adipose-derived stem cell laden alginate microspheres. Biomaterials, 33, 8802-8811.
70. Marx, R. E. (2004). Platelet-rich plasma: Evidence to support its use. Journal of Oral and Maxillofacial Surgery, 62, 489-496. (Pubitemid 38451232)
71. Mazzucco, L., Balbo, V., Cattana, E., Guaschino, R., & Borzini, P. (2009). Not every PRP-gel is born equal. Evaluation of growth factor availability for tissues through four PRP-gel preparations: Fibrinet® RegenPRP-Kit® Plateltex® and one manual procedure. Vox Sanguinis, 97, 110-118.
72. Mehta, M., Schmidt-Bleek, K., Duda, G. N., & Mooney, D. J. (2012). Biomaterial delivery of morphogens to mimic the natural healing cascade in bone. Advanced Drug Delivery Reviews, 64, 1257-1276.
73. Mooney, D. J., & Vandenburgh, H. (2008). Cell delivery mechanisms for tissue repair. Cell Stem Cell, 2, 205-213. (Pubitemid 351298597)
74. Muzzarelli, R. A. A. (1977). Chitin. Oxford: Pergamon Press.
75. Muzzarelli, R. A. A. (2009). Chitins and chitosans for the repair of wounded skin nerve cartilage and bone. Carbohydrate Polymers, 76, 167-182.
76. Muzzarelli, R. A. A. (2011). Chitosan composites with inorganics, morphogenetic proteins and stem cells, for bone regeneration. Carbohydrate Polymers, 83, 1433-1445.
77. Muzzarelli, R. A. A. (2010). Enhanced biochemical efficacy of oligochitosans and partially depolymerized chitosans. In F. Columbus (Ed.), Chitosan: Manufacture properties and usages. Hauppauge, NY: Nova Publishers Inc.
78. Muzzarelli, R. A. A., Biagini, G., Bellardini, M., Simonelli, L., Castaldini, C., & Fratto, G. (1993). Osteoconduction exerted by N-methylpyrrolidinone chitosan used in dental surgery. Biomaterials, 14, 39-43. (Pubitemid 23037169)
79. Muzzarelli, R. A. A., Boudrant, J., Meyer, D., Manno, N., DeMarchis, M., & Paoletti, M. G. (2012). A tribute to Henri Braconnot precursor of the carbohydrate polymers science on the chitin bicentennial. Carbohydrate Polymers, 87, 995-1012.
80. Muzzarelli, R. A. A., Greco, F., Busilacchi, A., Sollazzo, V., & Gigante, A. (2012). Chitosan hyaluronan and chondroitin sulfate in tissue engineering for cartilage regeneration: A review. Carbohydrate Polymers, 89, 723-739.
81. Muzzarelli, R. A. A., Mattioli-Belmonte, M., Tietz, C., Ferioli, G., Brunelli, M. A., Fini, M., et al. (1994). Stimulatory effect on bone formation exerted by a modified chitosan. Biomaterials, 15, 1075-1081. (Pubitemid 24345934)
82. Nandi, S. K., Kundu, B., & Basu, D. (2013). Protein growth factors loaded highly porous chitosan scaffold: A comparison of bone healing properties. Materials Science & Engineering C, 33, 1267-1275.
83. Okamoto, Y., Yano, R., Miyatake, K., Tomohiro, I., Shigemasa, Y., & Minami, S. (2003). Effects of chitin and chitosan on blood coagulation. Carbohydrate Polymers, 53, 337-342.
84. Oktay, E. O., Demiralp, B., Demiralp, B., Senel, S., Cevdet Akman, A., Eratalay, K., et al. (2010). Effects of platelet-rich plasma and chitosan combination on bone regeneration in experimental rabbit cranial defects. Journal of Oral Implantology, 36, 175-184.
85. Olney, J. W. (1969). Brain lesions obesity and other disturbances in mice treated with monosodium glutamate. Science, 164, 719-721.
86. Pahuja, P., Arora, S., & Pawar, P. (2012). Ocular drug delivery system: A reference to natural polymers. Expert Opinion on Drug Delivery, 9, 837-861.
87. Panuganti, S., Schlinker, A. C., Lindholm, P. F., Papoutsakis, E. T., & Miller, W. M. (2013). Three-stage ex vivo expansion of high-ploidy megakaryocytic cells: Toward large-scale platelet production. Tissue Engineering A, 19, 998-1014.
88. Paul, A., Chen, G. Y., Khan, A., Rao, V. T. S., Shum-Tim, D., & Prakash, S. (2013). Genipincross- linked microencapsulated human adipose stem cells augment transplant retention resulting in attenuation of chronically infarcted rat heart fibrosis and cardiac dysfunction. Cell Transplantation, 21, 2735-2751.
89. Paweletz, N. (2001). From Galen to Golgi: Birth of the life sciences in Italy. Nature Reviews Molecular Cell Biology, 2, 475-480. (Pubitemid 33680586)
90. Periayah, M. H., Halim, A. S., Hussein, A. R., Saad, A. Z. M., Rashid, A. H. A., & Noorsal, K. (2013). In vitro capacity of different grades of chitosan derivatives to induce platelet adhesion and aggregation. International Journal of Biological Macromolecules, 52, 244-249.
91. Picker, S. M. (2011). In-vitro assessment of platelet function. Transfusion and Apheresis Science, 44, 305-319.
92. Pozza, M., & Millner, R. W. J. (2011). Celox (chitosan) for haemostasis in massive traumatic bleeding: Experience in Afghanistan. European Journal of Emergency Medicine, 18, 31-33.
93. Pusateri, A. E., McCarthy, S. J., Gregory, K. W., Harris, R. A., Cardenas, L., McManus, A. T., et al. (2003). Effect of a chitosan-based hemostatic dressing on blood loss and survival in a model of severe venous hemorrhage and hepatic injury in swine. Journal of Trauma-Injury Infection and Critical Care, 54, 177-182. (Pubitemid 36113244)
94. Rappl, L. M. (2011). Effect of platelet rich plasma gel in a physiologically relevant platelet concentration on wounds in persons with spinal cord injury. International Wound Journal, 8, 187-195.
95. Ravi Kumar, M. N. V., Muzzarelli, R. A. A., Muzzarelli, C., Sashiwa, H., & Domb, A. J. (2004). Chitosan chemistry and pharmaceutical perspectives. Chemical Reviews, 104, 6017-6084. (Pubitemid 40025733)
96. Rehman, J., Traktuev, D., & Li, J. (2004). Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation, 109, 1292-1298. (Pubitemid 38372789)
97. Ribatti, D., & Crivellato, E. (2007). Giulio Bizzozero and the discovery of platelets. Leukemia Research, 31, 1339-1341. (Pubitemid 47225116)
98. Ripps, H., & Shen, W. (2012). Review: Taurine a very essential aminoacid. Molecular Vision, 18, 2673-2686.
99. Rodriguez-Merchan, E. C. (2012). Local fibrin glue and chitosan-based dressings in haemophilia surgery. Blood Coagulation Fibrinolysis, 23, 473-476.
100. Rossi, S., Faccendini, A., Bonferoni, M. C., Ferrari, F., Sandri, G., Del Fante, C., et al. (2012). Sponge-like dressings based on biopolymers for the delivery of platelet lysate to skin chronic wounds. International Journal of Pharmacy,. PMID: 22884830.
101. Saad Setta, H., Elshahat, A., Elsherbiny, K., Massoud, K., & Safe, I. (2011). Platelet-rich plasma versus platelet-poor plasma in the management of chronic diabetic foot ulcers: A comparative study. International Wound Journal, 8, 307-312.
102. Sadat, S., Gehmert, S., Song, Y. H., et al. (2007). The cardioprotective effect of mesenchymal stem cells is mediated by IGF-I and VEGF. Biochemical and Biophysical Research Communications, 363, 674-679. (Pubitemid 47513683)
103. Sahoo, N. G., Pan, Y. Z., Li, L., & He, C. B. (2013). Nanocomposites for bone tissue regeneration. Nanomedicine, 8, 639-653.
104. Salewski, R. P. F., Eftekharpour, E., & Fehlings, M. G. (2010). Are induced pluripotent stem cells the future of cell-based regenerative therapies for spinal cord injury? Journal of Cellular Physiology, 222, 515-521.
105. Sandri, G., Bonferoni, M. C., Rossi, S., Ferrari, F., Mori, M., Del Fante, C., et al. (2011). Platelet lysate formulations based on mucoadhesive polymers for the treatment of corneal lesions. Journal of Pharmacy and Pharmacology, 63, 189-198.
106. Santo, V. E., Duarte, A. R., Popa, E. G., Gomes, M. E., Mano, J. F., & Reis, R. L. (2012). Enhancement of osteogenic differentiation of human adipose derived stem cells by the controlled release of platelet lysates from hybrid scaffolds produced by supercritical fluid foaming. Journal of Controlled Release, 162, 19-27.
107. Santo, V. E., Gomes, M. E., Mano, J. F., & Reis, R. L. (2012). Chitosan-chondroitin sulphate nanoparticles for controlled delivery of platelet lysates in bone regenerative medicine. Journal of Tissue Engineering and Regenerative Medicine, 6, s47-s59, 3, http://dx.doi.org/10.1002/term.1519
108. Sarkar, M. R., Augat, P., Shefelbine, S. J., Schorlemmer, S., Huber-Lang, M., Claes, L., et al. (2006). Bone formation in a long bone defect model using a platelet-rich plasma-loaded collagen scaffold. Biomaterials, 27, 1817-1823. (Pubitemid 41759476)
109. Scevola, S., Nicoletti, G., Brenta, F., Isernia, P., Maestri, M., & Faga, A. (2010). Allogenic platelet gel in the treatment of pressure sores: A pilot study. International Wound Journal, 7, 184-190.
110. Shi, B. Y., Zhang, H., Shen, Z. Y., Bi, J. X., & Dai, S. (2013). Developing a chitosan supported imidazole Schiff-base for high-efficiency gene delivery. Polymer Chemistry, 4, 840-850.
111. Shi, Q., Zhao, J., Stagnaro, P., Yang, H., Luan, S., & Yin, J. (2012). Biocompatible polypropylene prepared by a combination of melt grafting and surface restructuring. Journal of Applied Polymer Science, 126, 929-938.
112. Soyer, T., Cakmak, M., Aslan, M. K., Senyucel, M., & Kisa, U. (2013). Use of autologous platelet rich fibrin in urethracutaneous fistula repair: Preliminary report. International Wound Journal, 10, 345-347.
113. St.Denis, T. G., Dai, T., Huang, Y. Y., & Hamblin, M. R. (2012). Wound healing properties of chitosan and its use in wound dressing biopharmaceuticals. In B. Sarmento, & J. DasNeves (Eds.), Chitosan-based systems for biopharmaceuticals (pp. 429-450). Chichester: Wiley.
114. Street, J., & Lenehan, B. (2009). Vascular endothelial growth factor regulates osteoblast survival: Evidence for an autocrine feedback mechanism. Journal of Orthopedic Surgery Research, 4, 19-25.
115. Sugamori, T., Iwase, H., Maeda, M., Inoue, Y., & Kurosawa, H. (2000). Local hemostatic effects of microcrystalline partially deacetylated chitin hydrochloride. Journal of Biomedical Materials Research, 49, 225-232.
116. Sweeney, I. R., Miraftab, M., & Collyer, G. (2012). A critical review of modern and emerging absorbent dressings used to treat exuding wounds. International Wound Journal, 9, 601-612.
117. Takahashi, K., & Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126, 663-676. (Pubitemid 44233629)
118. Takayama, N., & Eto, K. (2012). Pluripotent stem cells reveal the developmental biology of human megakaryocytes and provide a source of platelets for clinical application. Cellular and Molecular Life Sciences, 69, 3419-3428.
119. Traktuev, D. O., Merfeld-Clauss, S., & Li, J. (2008). A population of multipotent CD34- positive adipose stromal cells share pericyte and mesenchymal surface markers reside in a periendothelial location and stabilize endothelial networks. Circulation Research, 102, 77-85.
120. Tsai, W. B., Chen, Y. R., & Liu, H. L. (2013). RGD-conjugated crosslinked chitosan scaffolds for culture and osteogenic differentiation of mesenchymal stem cells. Journal of the Taiwan Institute of Chemical Engineers, 44, 1-7.
121. Tsuji, O., Miura, K., Okada, Y., Fujiyoshi, K., Mukaino, M., & Nagoshi, N. (2010). Therapeutic potential of appropriately evaluated safe-induced pluripotent stem cells for spinal cord injury. Proceedings of the National Academy of Sciences of the United States of America, 107, 12704-12709.
122. Vo, T. N., Kasper, F. K., & Mikos, A. G. (2012). Strategies for controlled delivery of growth factors and cells for bone regeneration. Advanced Drug Delivery Reviews, 64, 1292-1309.
123. Wang, P., Wang, Y., Kong, X., Man, Y., & Qu, Y. (2012). Wounded tissues and neurotoxicity of polyglutamate. Carbohydrate Polymers, 87, 1891-1892.
124. Wei, X. L., Chen, W., Mao, F., & Wang, Y. F. (2013). Effect of chitooligosaccharides on mice hematopoietic stem/progenitor cells. International Journal of Biological Macromolecules, 54, 71-75.
125. Weibrich, G., Kleis, W. K., & Hafner, G. (2002). Growth factor levels in the plateletrich plasma produced by 2 different methods: Curasan-type PRP kit versus PCCS PRP system. International Journal of Oral Maxillofacial Implants, 17, 184-190.
126. Weiner, B., Fischer, T., & Waxman, S. (2003). Hemostasis in the era of the chronic anticoagulated patient. Journal of Invasive Cardiology, 15, 669-674. (Pubitemid 37409448)
127. Whang, H. S., Kirsch, W., Zhu, Y. H., Yang, C. Z., & Hudson, S. M. (2005). Hemostatic agents derived from chitin and chitosan. Journal of Macromolecular Science-Polymer Reviews C, 45, 309-323.
128. Whitaker, M. J., Quirk, R. A., Howdle, S. M., & Shakesheff, K. M. (2001). Growth factor release from tissue engineering scaffolds. Journal of Pharmacy and Pharmacology, 531, 427-1437.
129. Wu, Y., Hu, Y., Cai, J., Ma, S., & Wang, X. P. (2008). Coagulation property of hyaluronic acid-collagen/chitosan complex film. Journal of Materials Science: Materials in Medicine, 19, 3621-3629.
130. Xia, W. J., Li, H., Wang, Z., Xu, Z., Fu, Y. S., Zhang, X. M., et al. (2011). Human platelet lysate supports ex vivo expansion and enhances osteogenic differentiation of human bone marrow-derived mesenchymal stem cells. Cell Biology International, 35, 639-643.
131. Xie, X., Wang, Y., Zhao, C., Guo, S. C., Liu, S., Jia, W., et al. (2012). Comparative evaluation of MSCs from bone marrow and adipose tissue seeded in PRP-derived scaffold for cartilage regeneration. Biomaterials, 33, 7008-7018.
132. Yan, S. F., Zhang, K. X., Liu, Z. W., Zhang, X., Gan, L., Cao, B., et al. (2013). Fabrication of poly(l-glutamic acid)/chitosan polyelectrolyte complex porous scaffolds for tissue engineering. Journal of Materials Chemistry B, 1, 1541-1551.
133. Zaky, S. H., Ottonello, A., Strada, P., Cancedda, R., & Mastrogiacomo, M. (2008). Platelet lysate favours in vitro expansion of human bone marrow stromal cells for bone and cartilage engineering. Journal of Tissue Engineering and Regeneration Medicine, 2, 472-481.
134. Zhang, H., Jia, X. L., Han, F. X., Zhao, J., Zhao, Y. H., Fan, Y. B., et al. (2013). Dual-delivery of VEGF and PDGF by double-layered electrospun membranes for blood vessel regeneration. Biomaterials, 34, 2202-2212.
135. Zhang, K., Zhang, Y., Yan, S., Gong, L., Wang, J., Chen, X., et al. (2013). Repair of an articular cartilage defect using adipose-derived stem cells loaded on a polyelectrolyte complex scaffold based on poly(l-glutamic acid) and chitosan. Acta Biomaterialia, http://dx.doi.org/10.1016/j.actbio.2013.03.025
136. Zhang, Y., Madhu, V., Dighe, A. S., Irvine, J. N., Jr., & Cui, Q. (2012). Osteogenic response of human adipose-derived stem cells to BMP-6 VEGF and combined VEGF plus BMP-6 in vitro. Growth Factors, 30, 333-343.
137. Zustiak, S. P., Wei, Y., & Leach, J. B. (2013). Protein-hydrogel interactions in tissue engineering: Mechanisms and applications. Tissue Engineering B, 19, 160-171.