Preparation, quality criteria, and properties of human blood platelet lysate supplements for ex vivo stem cell expansion

New Biotechnology

Volumn 32, Issue 1, 2015, Pages 199-211

  Shih, Daniel Tzu Bi ^a,b   Burnouf, Thierry ^c  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; DISEASE CONTROL; DISEASES; FLOWCHARTING; GOLD; PLATELETS; SAFETY ENGINEERING; STEM CELLS; TISSUE ENGINEERING;

CLINICAL APPLICATION; INFLAMMATORY DISEASE; MULTIPOTENT MESENCHYMAL STROMAL CELLS; PLATELET CONCENTRATES; QUALITY AND SAFETIES; REGENERATIVE MEDICINE; STEM CELL EXPANSION; TRANSLATIONAL MEDICINE;

CELL ENGINEERING;

PLATELET DERIVED GROWTH FACTOR; THROMBOCYTE CONCENTRATE; CULTURE MEDIUM;

APHERESIS; ARTICLE; BACTERIUM CONTAMINATION; BLOODBORNE BACTERIUM; CELL DIFFERENTIATION; CELL ISOLATION; CELL LYSATE; CELL PROLIFERATION; CELL SURVIVAL; CLINICAL TRIAL (TOPIC); GENE INACTIVATION; HUMAN; MESENCHYMAL STROMA CELL; NONHUMAN; SIGNAL TRANSDUCTION; STEM CELL EXPANSION; THROMBOCYTE; CULTURE MEDIUM; CULTURE TECHNIQUE; CYTOLOGY; DRUG EFFECTS; PROCEDURES; STANDARDS; STEM CELL;

BLOOD PLATELETS; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CULTURE MEDIA, SERUM-FREE; HUMANS; PLATELET-DERIVED GROWTH FACTOR; STEM CELLS;

EID: 84912139606     PISSN: 18716784     EISSN: 18764347     Source Type: Journal    
DOI: 10.1016/j.nbt.2014.06.001     Document Type: Article

References (158)

1. Barry F.P., Murphy J.M. Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 2004, 36:568-584.
2. Deans R.J., Moseley A.B. Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol 2000, 28:875-884.
3. Kassem M., Abdallah B.M. Human bone-marrow-derived mesenchymal stem cells: biological characteristics and potential role in therapy of degenerative diseases. Cell Tissue Res 2008, 331:157-163.
4. Le Blanc K., Ringden O. Immunomodulation by mesenchymal stem cells and clinical experience. J Internal Med 2007, 262:509-525.
5. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
6. Granero-Molto F., Weis J.A., Longobardi L., Spagnoli A. Role of mesenchymal stem cells in regenerative medicine: application to bone and cartilage repair. Expert Opin Biol Ther 2008, 8:255-268.
7. Berger M.G., Veyrat-Masson R., Rapatel C., Descamps S., Chassagne J., Boiret-Dupre N. Cell culture medium composition and translational adult bone marrow-derived stem cell research. Stem Cells 2006, 24:2888-2890.
8. Dimarakis I., Levicar N. Cell culture medium composition and translational adult bone marrow-derived stem cell research. Stem Cells 2006, 24:1407-1408.
9. Perez-Ilzarbe M., Diez-Campelo M., Aranda P., Tabera S., Lopez T., del Canizo C., et al. Comparison of ex vivo expansion culture conditions of mesenchymal stem cells for human cell therapy. Transfusion 2009, 49:1901-1910.
10. Sotiropoulou P.A., Perez S.A., Salagianni M., Baxevanis C.N., Papamichail M. Cell culture medium composition and translational adult bone marrow-derived stem cell research. Stem Cells 2006, 24:1409-1410.
11. Heiskanen A., Satomaa T., Tiitinen S., Laitinen A., Mannelin S., Impola U., et al. N-glycolylneuraminic acid xenoantigen contamination of human embryonic and mesenchymal stem cells is substantially reversible. Stem Cells 2007, 25:197-202.
12. Spees J.L., Gregory C.A., Singh H., Tucker H.A., Peister A., Lynch P.J., et al. Internalized antigens must be removed to prepare hypoimmunogenic mesenchymal stem cells for cell and gene therapy. Mol Ther 2004, 9:747-756.
13. Kievits F., Boerenkamp W.J., Ivanyi P. H-2-dependent binding of xenogeneic beta 2-microglobulin from culture media. J Immunol 1988, 140:4253-4255.
14. Mackensen A., Drager R., Schlesier M., Mertelsmann R., Lindemann A. Presence of IgE antibodies to bovine serum albumin in a patient developing anaphylaxis after vaccination with human peptide-pulsed dendritic cells. Cancer Immunol Immunother 2000, 49:152-156.
15. Selvaggi T.A., Walker R.E., Fleisher T.A. Development of antibodies to fetal calf serum with arthus-like reactions in human immunodeficiency virus-infected patients given syngeneic lymphocyte infusions. Blood 1997, 89:776-779.
16. Ivan A., Indrei L.L. Emergence of transmissible disorders, a continuous process - a new type of viral meningoencephalitis. Rev Med Chir Soc Med Nat Iasi 2000, 104:51-55.
17. Kaaden O.R., Eichhorn W., Essbauer S. Recent developments in the epidemiology of virus diseases. J Vet Med B: Infect Dis Vet Public Health 2002, 49:3-6.
18. Abbott A., Cyranoski D. Biologists seek to head off future sources of infection. Nature 2003, 423:3.
19. Ng S.K. Possible role of an animal vector in the SARS outbreak at Amoy Gardens. Lancet 2003, 362:570-572.
20. Gao R., Cao B., Hu Y., Feng Z., Wang D., Hu W., et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 2013, 368:1888-1897.
21. Anonymous Abu Dhabi 5 camel connection to new coronavirus?. Science 2013, 340. 127-127.
22. Robertson J.S. Bovine serum - regulatory issues. Dev Biol (Basel) 2006, 123:269-272. discussion 291-308.
23. Hill A.F., Desbruslais M., Joiner S., Sidle K.C.L., Gowland I., Collinge J., et al. The same prion strain causes vCJD and BSE. Nature 1997, 389:448-450.
24. CHMP Note for guidance on the use of bovine serum in the manufacture of human biological medicinal products 2003, European Medicine Agency, CPMP/BWP/1793/02. October. http://www.emea.eu.int.
25. WHO, 2006. WHO guidelines on tissue infectivity distribution in transmissible spongiform encephalopathies. http://www.who.int/bloodproducts.
26. Gstraunthaler G. Alternatives to the use of fetal bovine serum: serum-free cell culture. Altex Altern Tierexp 2003, 20:275-281.
27. van der Valk J., Mellor D., Brands R., Fischer R., Gruber F., Gstraunthaler G., et al. The humane collection of fetal bovine serum and possibilities for serum-free cell and tissue culture. Toxicol In Vitro 2004, 18:1-12.
28. Kuznetsov S.A., Friedenstein A.J., Robey P.G. Factors required for bone marrow stromal fibroblast colony formation in vitro. Br J Haematol 1997, 97:561-570.
29. Burnouf T. Recombinant plasma proteins. Vox Sang 2011, 100:68-83.
30. Grillberger L., Kreil T.R., Nasr S., Reiter M. Emerging trends in plasma-free manufacturing of recombinant protein therapeutics expressed in mammalian cells. Biotechnol J 2009, 4:186-201.
31. Fekete N., Rojewski M.T., Lotfi R., Schrezenmeier H. Essential components for ex vivo proliferation of mesenchymal stromal cells. Tissue Eng Part C Methods 2014, 20:129-139.
32. Bieback K. Platelet lysate as replacement for fetal bovine serum in mesenchymal stromal cell cultures. Transf Med Hemotherapy 2013, 40:326-335.
33. Blair P., Flaumenhaft R. Platelet alpha-granules: basic biology and clinical correlates. Blood Rev 2009, 23:177-189.
34. Kisucka J., Butterfield C.E., Duda D.G., Eichenberger S.C., Saffaripour S., Ware J., et al. Platelets and platelet adhesion support angiogenesis while preventing excessive hemorrhage. Proc Natl Acad Sci U S A 2006, 103:855-860.
35. Lucarelli E., Beccheroni A., Donati D., Sangiorgi L., Cenacchi A., Del Vento A.M., et al. Platelet-derived growth factors enhance proliferation of human stromal stem cells. Biomaterials 2003, 24:3095-3100.
36. Doucet C., Ernou I., Zhang Y., Llense J.R., Begot L., Holy X., et al. Platelet lysates promote mesenchymal stem cell expansion: a safety substitute for animal serum in cell-based therapy applications. J Cell Physiol 2005, 205:228-236.
37. Bieback K., Hecker A., Kocaomer A., Lannert H., Schallmoser K., Strunk D., et al. Human alternatives to fetal bovine serum for the expansion of mesenchymal stromal cells from bone marrow. Stem Cells 2009, 27:2331-2341.
38. Pawitan J.A. Platelet rich plasma in xeno-free stem cell culture: the impact of platelet count and processing method. Curr Stem Cell Res Ther 2012, 7:329-335.
39. Anonymous Guide to the preparation, use and quality assurance of blood components 2011, Council of Europe Publishing. 10th edition.
40. Kocaoemer A., Kern S., Kluter H., Bieback K. Human AB serum and thrombin-activated platelet-rich plasma are suitable alternatives to fetal calf serum for the expansion of mesenchymal stem cells from adipose tissue. Stem Cells 2007, 25:1270-1278.
41. Burnouf T., Goubran H.A., Chen T.M., Ou K.L., El-Ekiaby M., Radosevic M. Blood-derived biomaterials and platelet growth factors in regenerative medicine. Blood Rev 2013, 27:77-89.
42. Mazzucco L., Balbo V., Cattana E., Guaschino R., Borzini P. 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 Sang 2009, 97:110-118.
43. Burgstaler E.A. Blood component collection by apheresis. J Clin Apheresis 2006, 21:142-151.
44. Singh R.P., Marwaha N., Malhotra P., Dash S. Quality assessment of platelet concentrates prepared by platelet rich plasma-platelet concentrate, buffy coat poor-platelet concentrate (BC-PC) and apheresis-PC methods. Asian J Transfus Sci 2009, 3:86-94.
45. Pietersz R.N.I., van der Meer P.F., Steneker I., Hinloopen B., Dekker W.J.A., van Zanten A.P., et al. Preparation of leukodepleted platelet concentrates from pooled buffy coats: prestorage filtration with Autostop (TM) BC. Vox Sang 1999, 76:231-236.
46. van der Meer P., Pietersz R., Reesink H. Leucoreduced platelet concentrates in additive solution: an evaluation of filters and storage containers. Vox Sang 2001, 81:102-107.
47. Azuma H., Hirayama J., Akino M., Ikeda H. Platelet additive solution - electrolytes. Transf Apher Sci 2011, 44:277-281.
48. Eriksson L., Hogman C.F. Platelet concentrates in an additive solution prepared from pooled buffy coats. 1. In vitro studies. Vox Sang 1990, 59:140-145.
49. Fekete N., Gadelorge M., Furst D., Maurer C., Dausend J., Fleury-Cappellesso S., et al. Platelet lysate from whole blood-derived pooled platelet concentrates and apheresis-derived platelet concentrates for the isolation and expansion of human bone marrow mesenchymal stromal cells: production process, content and identification of active components. Cytotherapy 2012, 14:540-554.
50. Iudicone P., Fioravanti D., Bonanno G., Miceli M., Lavorino C., Totta P., et al. Pathogen-free, plasma-poor platelet lysate and expansion of human mesenchymal stem cells. J Transl Med 2014, 12:28.
51. Schallmoser K., Bartmann C., Rohde E., Reinisch A., Kashofer K., Stadelmeyer E., et al. Human platelet lysate can replace fetal bovine serum for clinical-scale expansion of functional mesenchymal stromal cells. Transfusion 2007, 47:1436-1446.
52. Jonsdottir-Buch S.M., Lieder R., Sigurjonsson O.E. Platelet lysates produced from expired platelet concentrates support growth and osteogenic differentiation of mesenchymal stem cells. PLoS One 2013, 8:e68984.
53. Commission E. Commission Directive 2003/94/EC of 8 October 2003 laying down the principles and guidelines of good manufacturing practice in respect of medicinal products doe human use and investigational medicinal products for human use. 14.10.2003. (Union, O. j. o. t. E. ed.) 2003, 22-26. European Commission.
54. WHO Guidelines on good manufacturing practices for blood establishments. Annex 4. WHO Tech Rep Series 2011, 961:148-214.
55. Allain J.P., Bianco C., Blajchman M.A., Brecher M.E., Busch M., Leiby D., et al. Protecting the blood supply from emerging pathogens: the role of pathogen inactivation. Transfus Med Rev 2005, 19:110-126.
56. Busch M.P., Kleinman S.H., Nemo G.J. Current and emerging infectious risks of blood transfusions. JAMA 2003, 289:959-962.
57. Dodd R.Y. Emerging pathogens and their implications for the blood supply and transfusion transmitted infections. Br J Haematol 2012, 159:135-142.
58. Lanteri M.C., Busch M.P. Dengue in the context of safe blood and global epidemiology: to screen or not to screen?. Transfusion 2012, 52:1634-1639.
59. Burnouf T., Radosevich M. Reducing the risk of infection from plasma products: specific preventative strategies. Blood Rev 2000, 14:94-110.
60. Prowse C., Ludlam C.A., Yap P.L. Human parvovirus B19 and blood products. Vox Sang 1997, 72:1-10.
61. Lefrere J.-J., Hewitt P. From mad cows to sensible blood transfusion: the risk of prion transmission by labile blood components in the United Kingdom and in France. Transfusion 2009, 49:797-812.
62. Llewelyn C.A., Hewitt P.E., Knight R.S.G., Amar K., Cousens S., Mackenzie J., et al. Possible transmission of variant Creutzfeldt-Jakob disease by blood transfusion. Lancet 2004, 363:417-421.
63. Burnouf T., Padilla A. Current strategies to prevent transmission of prions by human plasma derivatives. Transf Clin Biol 2006, 13:320-328.
64. Gregori L., McCombie N., Palmer D., Birch P., Sowemimo-Coker S.O., Giulivi A., et al. Effectiveness of leucoreduction for removal of infectivity of transmissible spongiform encephalopathies from blood. Lancet 2004, 364:529-531.
65. Vamvakas E.C. Universal white blood cell reduction in Europe: has transmission of variant Creutzfeldt-Jakob disease been prevented?. Transf Med Rev 2011, 25:133-144.
66. Cancelas J.A., Rugg N., Pratt P.G., Worsham D.N., Pehta J.C., Banks K., et al. Infusion of P-Capt prion-filtered red blood cell products demonstrate acceptable in vivo viability and no evidence of neoantigen formation. Transfusion 2011, 51:2228-2236.
67. Edgeworth J.A., Farmer M., Sicilia A., Tavares P., Beck J., Campbell T., et al. Detection of prion infection in variant Creutzfeldt-Jakob disease: a blood-based assay. Lancet 2011, 377:487-493.
68. Busch M.P., Glynn S.A., Stramer S.L., Strong D.M., Caglioti S., Wright D.J., et al. A new strategy for estimating risks of transfusion-transmitted viral infections based on rates of detection of recently infected donors. Transfusion 2005, 45:254-264.
69. Dodd R.Y. Current risk for transfusion transmitted infections. Curr Opin Hematol 2007, 14:671-676.
70. Zou S.M., Stramer S.L., Dodd R.Y. Donor testing and risk: current prevalence, incidence, and residual risk of transfusion-transmissible agents in US allogeneic donations. Transf Med Rev 2012, 26:119-128.
71. de Mendoza C., Altisent C., Aznar J.A., Batlle J., Soriano V. Emerging viral infections - a potential threat for blood supply in the 21st century. Aids Rev 2012, 14:279-289.
72. Reesink H.W., Panzer S., McQuilten Z.K., Wood E.M., Marks C., Wendel S., et al. Pathogen inactivation of platelet concentrates. Vox Sang 2010, 99:85-95.
73. Lin L., Cook D.N., Wiesehahn G.P., Alfonso R., Behrman B., Cimino G.D., et al. Photochemical inactivation of viruses and bacteria in platelet concentrates by use of a novel psoralen and long-wavelength ultraviolet light. Transfusion 1997, 37:423-435.
74. Lin L., Hanson C.V., Alter H.J., Jauvin V., Bernard K.A., Murthy K.K., et al. Inactivation of viruses in platelet concentrates by photochemical treatment with amotosalen and long-wavelength ultraviolet light. Transfusion 2005, 45:580-590.
75. Klein H.G. Pathogen inactivation technology: cleansing the blood supply. J Intern Med 2005, 257:224-237.
76. Ruane P.H., Edrich R., Gampp D., Keil S.D., Leonard R.L., Goodrich R.P. Photochemical inactivation of selected viruses and bacteria in platelet concentrates using riboflavin and light. Transfusion 2004, 44:877-885.
77. Corbin F. Pathogen inactivation of blood components: current status and introduction of an approach using riboflavin as a photosensitizer. Int J Hematol 2002, 76(Suppl 2):253-257.
78. Goodrich R.P. The use of riboflavin for the inactivation of pathogens in blood products. Vox Sang 2000, 78(Suppl 2):211-215.
79. AuBuchon J.P., Herschel L., Roger J., Taylor H., Whitley P., Li J.Z., et al. Efficacy of apheresis platelets treated with riboflavin and ultraviolet light for pathogen reduction. Transfusion 2005, 45:1335-1341.
80. Castrillo A., Cardoso M., Rouse L. Treatment of buffy coat platelets in platelet additive solution with the mirasol (R) pathogen reduction technology system. Transf Med Hemother 2013, 40:44-48.
81. Cookson P., Thomas S., Marschner S., Goodrich R., Cardigan R. In vitro quality of single-donor platelets treated with riboflavin and ultraviolet light and stored in platelet storage medium for up to 8 days. Transfusion 2012, 52:983-994.
82. Mohr H., Steil L., Gravemann U., Thiele T., Hammer E., Greinacher A., et al. A novel approach to pathogen reduction in platelet concentrates using short-wave ultraviolet light. Transfusion 2009, 49:2612-2624.
83. Stahle M., Carlsson B., Le Blanc K., Korsgren O., Knutson F. Photochemical pathogen inactivation of human serum enables its large-scale application in clinical cell transplantation. Vox Sang 2010, 98:e364-e365.
84. Stahle M.U., Brandhorst D., Korsgren O., Knutson F. Pathogen inactivation of human serum facilitates its clinical use for islet cell culture and subsequent transplantation. Cell Transpl 2011, 20:775-781.
85. Horowitz B., Bonomo R., Prince A.M., Chin S.N., Brotman B., Shulman R.W. Solvent/detergent-treated plasma: a virus-inactivated substitute for fresh frozen plasma. Blood 1992, 79:826-831.
86. Burnouf T., Tseng Y.H., Kuo Y.P., Su C.Y. Solvent/detergent treatment of platelet concentrates enhances the release of growth factors. Transfusion 2008, 48:1090-1098.
87. Su C.Y., Kuo Y.P., Lin Y.C., Huang C.T., Tseng Y.H., Burnouf T. A virally inactivated functional growth factor preparation from human platelet concentrates. Vox Sang 2009, 97:119-128.
88. Shih D.T., Chen J.C., Chen W.Y., Kuo Y.P., Su C.Y., Burnouf T. Expansion of adipose tissue mesenchymal stromal progenitors in serum-free medium supplemented with virally inactivated allogeneic human platelet lysate. Transfusion 2011, 51:770-778.
89. Dichtelmuller H.O., Biesert L., Fabbrizzi F., Gajardo R., Groner A., von Hoegen I., et al. Robustness of solvent/detergent treatment of plasma derivatives: a data collection from Plasma Protein Therapeutics Association member companies. Transfusion 2009, 49:1931-1943.
90. Blajchman M.A., Beckers E.A., Dickmeiss E., Lin L., Moore G., Muylle L. Bacterial detection of platelets: current problems and possible resolutions. Transf Med Rev 2005, 19:259-272.
91. de Korte D., Marcelis J.H., Soeterboek A.M. Determination of the degree of bacterial contamination of whole-blood collections using an automated microbe-detection system. Transfusion 2001, 41:815-818.
92. Blajchman M.A. Bacterial contamination of cellular blood components: risks, sources and control. Vox Sang 2004, 87(Suppl1):98L 103.
93. Montag T. Strategies of bacteria screening in cellular blood components. Clin Chem Lab Med 2008, 46:926-932.
94. Jenkins C., Ramirez-Arcos S., Goldman M., Devine D.V. Bacterial contamination in platelets: incremental improvements drive down but do not eliminate risk. Transfusion 2011, 51:2555-2565.
95. Chou M.L., Wu Y.W., Su C.Y., Lee L.W., Burnouf T. Impact of solvent/detergent treatment of plasma on transfusion-relevant bacteria. Vox Sang 2012, 102:277-284.
96. Mininkova A.I. Investigation of platelets by the flow cytofluorometric technique (a review of literature). Part 2. Klinicheskaia Laboratornaia Diagnostika 2011, 25-30.
97. Centeno C.J., Schultz J.R., Cheever M., Freeman M., Faulkner S., Robinson B., et al. Safety and complications reporting update on the re-implantation of culture-expanded mesenchymal stem cells using autologous platelet lysate technique. Curr Stem Cell Res Therapy 2011, 6:368-378.
98. Mazzucco L., Balbo V., Cattana E., Borzini P. Platelet-rich plasma and platelet gel preparation using Plateltex(R). Vox Sang 2008, 94:202-208.
99. Horn P., Bokermann G., Cholewa D., Bork S., Walenda T., Koch C., et al. Impact of individual platelet lysates on isolation and growth of human mesenchymal stromal cells. Cytotherapy 2010, 12:888-898.
100. Lohmann M., Walenda G., Hemeda H., Joussen S., Drescher W., Jockenhoevel S., et al. Donor age of human platelet lysate affects proliferation and differentiation of mesenchymal stem cells. PLoS One 2012, 7.
101. Schallmoser K., Strunk D. Generation of a pool of human platelet lysate and efficient use in cell culture. Methods Mol Biol 2013, 946:349-362.
102. Janetzko K., Kluter H., van Waeg G., Eichler H. Fully automated processing of buffy-coat-derived pooled platelet concentrates. Transfusion 2004, 44:1052-1058.
103. Flemming A., Schallmoser K., Strunk D., Stolk M., Volk H.D., Seifert M. Immunomodulative efficacy of bone marrow-derived mesenchymal stem cells cultured in human platelet lysate. J Clin Immunol 2011, 31:1143-1156.
104. Chen B., Sun H.H., Wang H.G., Kong H., Chen F.M., Yu Q. The effects of human platelet lysate on dental pulp stem cells derived from impacted human third molars. Biomaterials 2012, 33:5023-5035.
105. Blande I.S., Bassaneze V., Lavini-Ramos C., Fae K.C., Kalil J., Miyakawa A.A., et al. Adipose tissue mesenchymal stem cell expansion in animal serum-free medium supplemented with autologous human platelet lysate. Transfusion 2009, 49:2680-2685.
106. Bernardo M.E., Avanzini M.A., Perotti C., Cometa A.M., Moretta A., Lenta E., et al. Optimization of in vitro expansion of human multipotent mesenchymal stromal cells for cell-therapy approaches: further insights in the search for a fetal calf serum substitute. J Cell Physiol 2007, 211:121-130.
107. Chevallier N., Anagnostou F., Zilber S., Bodivit G., Maurin S., Barrault A., et al. Osteoblastic differentiation of human mesenchymal stem cells with platelet lysate. Biomaterials 2010, 31:270-278.
108. Bernardi M., Albiero E., Alghisi A., Chieregato K., Lievore C., Madeo D., et al. Production of human platelet lysate by use of ultrasound for ex vivo expansion of human bone marrow-derived mesenchymal stromal cells. Cytotherapy 2013, 15:920-929.
109. Burnouf T., Lee C.Y., Luo C.W., Kuo Y.P., Chou M.L., Wu Y.W., et al. Human blood-derived fibrin releasates: composition and use for the culture of cell lines and human primary cells. Biologicals 2012, 40:21-30.
110. Hemeda H., Kalz J., Walenda G., Lohmann M., Wagner W. Heparin concentration is critical for cell culture with human platelet lysate. Cytotherapy 2013, 15:1174-1181.
111. Mojica-Henshaw M.P., Jacobson P., Morris J., Kelley L., Pierce J., Boyer M., et al. Serum-converted platelet lysate can substitute for fetal bovine serum in human mesenchymal stromal cell cultures. Cytotherapy 2013, 15:1458-1468.
112. Borzini P., Mazzucco L. Platelet gels and releasates. Curr Opin Hematol 2005, 12:473-479.
113. Mizuno N., Shiba H., Ozeki Y., Mouri Y., Niitani M., Inui T., et al. Human autologous serum obtained using a completely closed bag system as a substitute for foetal calf serum in human mesenchymal stem cell cultures. Cell Biol Int 2006, 30:521-524.
114. Capelli C., Domenghini M., Borleri G., Bellavita P., Poma R., Carobbio A., et al. Human platelet lysate allows expansion and clinical grade production of mesenchymal stromal cells from small samples of bone marrow aspirates or marrow filter washouts. Bone Marrow Transpl 2007, 40:785-791.
115. Salvade A., Della Mina P., Gaddi D., Gatto F., Villa A., Bigoni M., et al. Characterization of platelet lysate cultured mesenchymal stromal cells and their potential use in tissue-engineered osteogenic devices for the treatment of bone defects. Tissue Eng Part C Methods 2010, 16:201-214.
116. Werner S., Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev 2003, 83:835-870.
117. Bennett N.T., Schultz G.S. Growth-factors and wound healing - biochemical properties of growth factors and their receptors. Am J Surg 1993, 165:728-737.
118. Liu Y.W., Kalen A., Risto O., Wahlstrom O. Fibroblast proliferation due to exposure to a platelet concentrate in vitro is pH dependent. Wound Repair Regeneration 2002, 10:336-340.
119. Anitua E., Andia I., Ardanza B., Nurden P., Nurden A.T. Autologous platelets as a source of proteins for healing and tissue regeneration. Thromb Haemost 2004, 91:4-15.
120. Sanchez-Gonzalez D.J., Mendez-Bolaina E., Trejo-Bahena N.I. Platelet-rich plasma peptides: key for regeneration. Int J Peptides 2012, 2012. 532519-532519.
121. Siljander P.R.M. Platelet-derived microparticles - an updated perspective. Thromb Res 2011, 127:S30-S33.
122. Borzini P., Mazzucco L. Platelet-rich plasma (PRP) and platelet derivatives for topical therapy. What is true from the biologic view point?. ISBT Sci Series 2007, 2:272-281.
123. Cole B.J., Seroyer S.T., Filardo G., Bajaj S., Fortier L.A. Platelet-rich plasma: where are we now and where are we going?. Sports Health 2010, 2:203-210.
124. Eppley B.L., Woodell J.E., Higgins J. Platelet quantification and growth factor analysis from platelet-rich plasma: implications for wound healing. Plastic Reconstruct Surg 2004, 114:1502-1508.
125. Frechette J.P., Martineau I., Gagnon G. Platelet-rich plasmas: growth factor content and roles in wound healing. J Dental Res 2005, 84:434-439.
126. Anitua E., Sanchez M., Orive G., Andia I. The potential impact of the preparation rich in growth factors (PRGF) in different medical fields. Biomaterials 2007, 28:4551-4560.
127. Celotti F., Colciago A., Negri-Cesi P., Pravettoni A., Zaninetti R., Sacchi M.C. Effect of platelet-rich plasma on migration and proliferation of SaOS-2 osteoblasts: role of platelet-derived growth factor and transforming growth factor-beta. Wound Repair Regen 2006, 14:195-202.
128. Driver V.R., Hanft J., Fylling C.P., Beriou J.M., Autologel Diabetic Foot Ulcer Study G. A prospective, randomized, controlled trial of autologous platelet-rich plasma gel for the treatment of diabetic foot ulcers. Ostomy/wound Manage 2006, 52:68-70. 72, 74 passim.
129. Knighton D.R., Ciresi K., Fiegel V.D., Schumerth S., Butler E., Cerra F. Stimulation of repair in chronic, nonhealing, cutaneous ulcers using platelet-derived wound healing formula. Surg Gynecol Obstet 1990, 170:56-60.
130. Knighton D.R., Ciresi K.F., Fiegel V.D., Austin L.L., Butler E.L. Classification and treatment of chronic nonhealing wounds. Successful treatment with autologous platelet-derived wound healing factors (PDWHF). Anna Surg 1986, 204:322-330.
131. McAleer J.P., Sharma S., Kaplan E.M., Persich G. Use of autologous platelet concentrate in a nonhealing lower extremity wound. Adv Skin Wound Care 2006, 19:354-363.
132. O'Connell S.M., Impeduglia T., Hessler K., Wang X.J., Carroll R.J., Dardik H. Autologous platelet-rich fibrin matrix as cell therapy in the healing of chronic lower-extremity ulcers. Wound Repair Regen 2008, 16:749-756.
133. Kinzebach S., Dietz L., Kluter H., Thierse H.J., Bieback K. Functional and differential proteomic analyses to identify platelet derived factors affecting ex vivo expansion of mesenchymal stromal cells. BMC Cell Biol 2013, 14:48.
134. Pons J., Huang Y., Arakawa-Hoyt J., Washko D., Takagawa J., Ye J., et al. VEGF improves survival of mesenchymal stem cells in infarcted hearts. Biochem Biophys Res Commun 2008, 376:419-422.
135. Tang J., Wang J., Zheng F., Kong X., Guo L., Yang J., et al. Combination of chemokine and angiogenic factor genes and mesenchymal stem cells could enhance angiogenesis and improve cardiac function after acute myocardial infarction in rats. Mol Cell Biochem 2010, 339:107-118.
136. Wang X.H., Hu Q.S., Mansoor A., Lee J., Wang Z.L., Lee T., et al. Bioenergetic and functional consequences of stem cell-based VEGF delivery in pressure-overloaded swine hearts. Am J Physiol-Heart Circ Physiol 2006, 290:H1393-H1405.
137. Bonewald L.F., Dallas S.L. Role of active and latent transforming growth factor beta in bone formation. J Cell Biochem 1994, 55:350-357.
138. Canalis E., McCarthy T.L., Centrella M. Effects of platelet-derived growth factor on bone formation in vitro. J Cell Physiol 1989, 140:530-537.
139. van der Kraan P.M., Davidson E.N.B., Blom A., van den Berg W.B. TGF-beta signaling in chondrocyte terminal differentiation and osteoarthritis. Modulation and integration of signaling pathways through receptor-Smads. Osteoarthritis Cartilage 2009, 17:1539-1545.
140. Longobardi L., O'Rear L., Aakula S., Johnstone B., Shimer K., Chytil A., et al. Effect of IGF-1 in the chondrogenesis of bone marrow mesenchymal stem cells in the presence or absence of TGF-beta signaling. J Bone Miner Res 2006, 21:626-636.
141. Ogawa T., Akazawa T., Tabata Y. In vitro proliferation and chondrogenic differentiation of rat bone marrow stem cells cultured with gelatin hydrogel microspheres for TGF-beta 1 release. J Biomater Sci-Polym Ed 2010, 21:609-621.
142. Weiss S., Hennig T., Bock R., Steck E., Richter W. Impact of growth factors and PTHrP on early and late chondrogenic differentiation of human mesenchymal stem cells. J Cell Physiol 2010, 223:84-93.
143. Luu H.H., Song W.-X., Luo X., Manning D., Luo J., Deng Z.-L., et al. Distinct roles of bone morphogenetic proteins in osteogenic differentiation of mesenchymal stem cells. J Orthopaedic Res 2007, 25:665-677.
144. Chang S.C.N., Chung H.-Y., Tai C.-L., Chen P.K.T., Lin T.-M., Jeng L.-B. Repair of large cranial defects by hBMP-2 expressing bone marrow stromal cells: comparison between alginate and collagen type I systems. J Biomed Mater Res Part A 2010, 94A:433-441.
145. Lou J.R., Xu F., Merkel K., Manske P. Gene therapy: adenovirus-mediated human bone morphogenetic protein-2 gene transfer induces mesenchymal progenitor cell proliferation and differentiation in vitro and bone formation in vivo. J Orthopaedic Res 1999, 17:43-50.
146. Stewart A., Guan H., Yang K. BMP-3 promotes mesenchymal stem cell proliferation through the TGF-beta/activin signaling pathway. J Cell Physiol 2010, 223:658-666.
147. Simmons C.A., Alsberg E., Hsiong S., Kim W.J., Mooney D.J. Dual growth factor delivery and controlled scaffold degradation enhance in vivo bone formation by transplanted bone marrow stromal cells. Bone 2004, 35:562-569.
148. Valcourt U., Gouttenoire J., Moustakas A., Herbage D., Mallein-Gerin F. Functions of transforming growth factor-beta family type I receptors and smad proteins in the hypertrophic maturation and osteoblastic differentiation of chondrocytes. J Biol Chem 2002, 277:33545-33558.
149. Zhang Y.E. Non-Smad pathways in TGF-beta signaling. Cell Res 2009, 19:128-139.
150. Lou J., Tu Y., Li S., Manske P.R. Involvement of ERK in BMP-2 induced osteoblastic differentiation of mesenchymal progenitor cell line C3H10T1/2. Biochem Biophys Res Commun 2000, 268:757-762.
151. Herrmann J.L., Wang Y., Abarbanell A.M., Weil B.R., Tan J., Meldrum D.R. Preconditioning mesenchymal stem cells with transforming growth factor-alpha improves mesenchymal stem cell-mediated cardioprotection. Shock 2010, 33:24-30.
152. Mahmood A., Lu D.Y., Wang L., Chopp M. Intracerebral transplantation of marrow stromal cells cultured with neurotrophic factors promotes functional recovery in adult rats subjected to traumatic brain injury. J Neurotrauma 2002, 19:1609-1617.
153. Krausgrill B., Vantler M., Burst V., Raths M., Halbach M., Frank K., et al. Influence of cell treatment with PDGF-BB and reperfusion on cardiac persistence of mononuclear and mesenchymal bone marrow cells after transplantation into acute myocardial infarction in rats. Cell Transpl 2009, 18:847-853.
154. Forte G., Minieri M., Cossa P., Antenucci D., Sala M., Gnocchi V., et al. Hepatocyte growth factor effects on mesenchymal stem cells: proliferation, migration, and differentiation. Stem Cells 2006, 24:23-33.
155. Fan V.H., Au A., Tamama K., Littrell R., Richardson L.B., Wright J.W., et al. Tethered epidermal growth factor provides a survival advantage to mesenchymal stem cells. Stem Cells 2007, 25:1241-1251.
156. WHO Blood Safety - Key global fact and figures in 2011. (Organization, W. H. ed.) 2011, World Health Organization.
157. Dietz A.B., Padley D.J., Gastineau D.A. Infrastructure development for human cell therapy translation. Clin Pharmacol Ther 2007, 82:320-324.
158. WHO WHO Expert Committee on biological standardization - WHO Recommendations for the production, control and regulation of human plasma for fractionation. World Health Organization Tech Rep Series 2007, 1-340, back cover.