Optimization of pre-transplantation conditions to enhance the efficacy of mesenchymal stem cells

International Journal of Biological Sciences

Volumn 11, Issue 3, 2015, Pages 324-334

  Haque, Nazmul ^a   Abu Kasim, Noor Hayaty ^a   Rahman, Mohammad Tariqur ^b  

^a UNIVERSITY OF MALAYA   (Malaysia)

^b INTERNATIONAL ISLAMIC UNIVERSITY MALAYSIA   (Malaysia)

Author keywords

Allogeneic; Autologous; Chemokine receptors; Hyper immunogenicity; Mesenchymal stem cell; Xenogenic

Indexed keywords

CULTURE MEDIUM;

BIOLOGICAL THERAPY; CELL DIFFERENTIATION; CELL SURVIVAL; CULTURE MEDIUM; CULTURE TECHNIQUE; CYTOLOGY; HUMAN; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; REGENERATIVE MEDICINE;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL SURVIVAL; CELL- AND TISSUE-BASED THERAPY; CULTURE MEDIA; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; REGENERATIVE MEDICINE;

EID: 84922367128     PISSN: 14492288     EISSN: None     Source Type: Journal    
DOI: 10.7150/ijbs.10567     Document Type: Article

References (154)

1. Fuchs E, Chen T. A matter of life and death: self-renewal in stem cells. EMBO Rep. 2013; 14: 39-48.
2. Caplan AI. MSCs as Therapeutics. Mesenchymal Stromal Cells. Springer; 2013: 79-90.
3. Ramírez M, Lucia A, Gómez-Gallego F, Esteve-Lanao J, Pérez-Martínez A, Foster C, et al. Mobilisation of mesenchymal cells into blood in response to skeletal muscle injury. British journal of sports medicine. 2006; 40: 719-22.
4. Carbonare LD, Valenti MT, Zanatta M, Donatelli L, Lo Cascio V. Circulating mesenchymal stem cells with abnormal osteogenic differentiation in patients with osteoporosis. Arthritis & Rheumatism. 2009; 60: 3356-65.
5. Wang Y, Johnsen HE, Mortensen S, Bindslev L, Ripa RS, HaacK-Sørensen M, et al. Changes in circulating mesenchymal stem cells, stem cell homing factor, and vascular growth factors in patients with acute ST elevation myocardial infarction treated with primary percutaneous coronary intervention. Heart. 2006; 92: 768-74.
6. Paczkowska E, Kucia M, Koziarska D, Halasa M, Safranow K, Masiuk M, et al. Clinical evidence that very small embryonic-like stem cells are mobilized into peripheral blood in patients after stroke. Stroke. 2009; 40: 1237-44.
7. Hatzistergos KE, Quevedo H, Oskouei BN, Hu Q, Feigenbaum GS, Margitich IS, et al. Bone Marrow Mesenchymal Stem Cells Stimulate Cardiac Stem Cell Proliferation and DifferentiationNovelty and Significance. Circulation research. 2010; 107: 913-22.
8. Kucia M, Zhang Y, Reca R, Wysoczynski M, Machalinski B, Majka M, et al. Cells enriched in markers of neural tissue-committed stem cells reside in the bone marrow and are mobilized into the peripheral blood following stroke. Leukemia. 2006; 20: 18-28.
9. Levi B, Hyun JS, Montoro DT, Lo DD, Chan CK, Hu S, et al. In vivo directed differentiation of pluripotent stem cells for skeletal regeneration. Proceedings of the National Academy of Sciences. 2012; 109: 20379-84.
10. Robertson JA. Embryo stem cell research: ten years of controversy. The Journal of Law, Medicine & Ethics. 2010; 38: 191-203.
11. Okita K, Yamakawa T, Matsumura Y, Sato Y, Amano N, Watanabe A, et al. An efficient nonviral method to generate integration-free human-induced pluripotent stem cells from cord blood and peripheral blood cells. Stem Cells. 2013; 31: 458-66.
12. Wang Y, Liu J, Tan X, Li G, Gao Y, Liu X, et al. Induced Pluripotent Stem Cells from Human Hair Follicle Mesenchymal Stem Cells. Stem Cell Reviews and Reports. 2012;: 1-10.
13. Polo JM, Liu S, Figueroa ME, Kulalert W, Eminli S, Tan KY, et al. Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat Biotechnol. 2010; 28: 848-55.
14. Liang G, Zhang Y. Genetic and epigenetic variations in iPSCs: potential causes and implications for application. Cell stem cell. 2013; 13: 149-59.
15. Caplan AI, Correa D. The MSC: an injury drugstore. Cell Stem Cell. 2011; 9: 11-5.
16. Govindasamy V, Ronald V, Abdullah A, Nathan KRG, Aziz ZACA, Abdullah M, et al. Differentiation of dental pulp stem cells into islet-like aggregates. Journal of dental research. 2011; 90: 646-52.
17. Estrada J, Torres Y, Benguría A, Dopazo A, Roche E, Carrera-Quintanar L, et al. Human mesenchymal stem cell-replicative senescence and oxidative stress are closely linked to aneuploidy. Cell death & disease. 2013; 4: e691.
18. Haque N, Rahman MT, Abu Kasim NH, Alabsi AM. Hypoxic Culture Conditions as a Solution for Mesenchymal Stem Cell Based Regenerative Therapy. The Scientific World Journal. 2013; 2013: 12.
19. Brown SE, Tong W, Krebsbach PH. The derivation of mesenchymal stem cells from human embryonic stem cells. Cells Tissues Organs. 2009; 189: 256-60.
20. Lian Q, Zhang Y, Zhang J, Zhang HK, Wu X, Zhang Y, et al. Functional mesenchymal stem cells derived from human induced pluripotent stem cells attenuate limb ischemia in mice. Circulation. 2010; 121: 1113-23.
21. Villa-Diaz LG, Brown SE, Liu Y, Ross AM, Lahann J, Parent JM, et al. Derivation of mesenchymal stem cells from human induced pluripotent stem cells cultured on synthetic substrates. Stem Cells. 2012; 30: 1174-81.
22. Liu Y, Goldberg AJ, Dennis JE, Gronowicz GA, Kuhn LT. One-Step Derivation of Mesenchymal Stem Cell (MSC)-Like Cells from Human Pluripotent Stem Cells on a Fibrillar Collagen Coating. PLoS ONE. 2012; 7: e33225.
23. Zou L, Luo Y, Chen M, Wang G, Ding M, Petersen CC, et al. A simple method for deriving functional MSCs and applied for osteogenesis in 3D scaffolds. Sci Rep. 2013; 3.
24. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. science. 1999; 284: 143-7.
25. Azizi SA, Stokes D, Augelli BJ, DiGirolamo C, Prockop DJ. Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats—similarities to astrocyte grafts. Proceedings of the National Academy of Sciences. 1998; 95: 3908-13.
26. Jin HK, Carter JE, Huntley GW, Schuchman EH. Intracerebral transplantation of mesenchymal stem cells into acid sphingomyelinase-deficient mice delays the onset of neurological abnormalities and extends their life span. Journal of Clinical Investigation. 2002; 109: 1183-92.
27. Shake JG, Gruber PJ, Baumgartner WA, Senechal G, Meyers J, Redmond JM, et al. Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects. The Annals of thoracic surgery. 2002; 73: 1919-26.
28. Kim N, Cho S-G. Clinical applications of mesenchymal stem cells. The Korean journal of internal medicine. 2013; 28: 387-402.
29. Volarevic V, Arsenijevic N, Lukic ML, Stojkovic M. Concise review: Mesenchymal stem cell treatment of the complications of diabetes mellitus. Stem Cells. 2011; 29: 5-10.
30. Malliaras K, Marban E. Cardiac cell therapy: where we've been, where we are, and where we should be headed. Br Med Bull. 2011; 98: 161-85.
31. Guo L, Ge J, Wang S, Zhou Y, Wang X, Wu Y. A novel method for efficient delivery of stem cells to the ischemic brain. Stem Cell Research & Therapy. 2013; 4: 116.
32. Lu S-s, Liu S, Zu Q-q, Xu X-q, Yu J, Wang J-w, et al. In Vivo MR Imaging of Intraarterially Delivered Magnetically Labeled Mesenchymal Stem Cells in a Canine Stroke Model. PloS one. 2013; 8: e54963.
33. Kean TJ, Lin P, Caplan AI, Dennis JE. MSCs: Delivery Routes and Engraftment, Cell-Targeting Strategies, and Immune Modulation. Stem Cells International. 2013; 2013: 13.
34. Liu H, Liu S, Li Y, Wang X, Xue W, Ge G, et al. The role of SDF-1-CXCR4/CXCR7 axis in the therapeutic effects of hypoxia-preconditioned mesenchymal stem cells for renal ischemia/reperfusion injury. PloS one. 2012; 7: e34608.
35. Saller MM, Prall WC, Docheva D, Schonitzer V, Popov T, Anz D, et al. Increased stemness and migration of human mesenchymal stem cells in hypoxia is associated with altered integrin expression. Biochemical and Biophysical Research Communications. 2012; 423: 379-85.
36. Hung SP, Ho JH, Shih YRV, Lo T, Lee OK. Hypoxia promotes proliferation and osteogenic differentiation potentials of human mesenchymal stem cells. Journal of Orthopaedic Research. 2012; 30: 260-6.
37. Estrada J, Albo C, Benguría A, Dopazo A, López-Romero P, Carrera-Quintanar L, et al. Culture of human mesenchymal stem cells at low oxygen tension improves growth and genetic stability by activating glycolysis. Cell Death & Differentiation. 2012; 19: 743-55.
38. Sakamoto N, Tsuji K, Muul LM, Lawler AM, Petricoin EF, Candotti F, et al. Bovine apolipoprotein B-100 is a dominant immunogen in therapeutic cell populations cultured in fetal calf serum in mice and humans. Blood. 2007; 110: 501-8.
39. Basciano L, Nemos C, Foliguet B, de Isla N, de Carvalho M, Tran N, et al. Long term culture of mesenchymal stem cells in hypoxia promotes a genetic program maintaining their undifferentiated and multipotent status. BMC cell biology. 2011; 12: 12.
40. Grayson WL, Zhao F, Bunnell B, Ma T. Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochemical and Biophysical Research Communications. 2007; 358: 948-53.
41. Connick P, Kolappan M, Patani R, Scott MA, Crawley C, He XL, et al. The mesenchymal stem cells in multiple sclerosis (MSCIMS) trial protocol and baseline cohort characteristics: an open-label pre-test: post-test study with blinded outcome assessments. Trials. 2011; 12: 62.
42. Connick P, Kolappan M, Crawley C, Webber DJ, Patani R, Michell AW, et al. Autologous mesenchymal stem cells for the treatment of secondary progressive multiple sclerosis: an open-label phase 2a proof-of-concept study. Lancet Neurol. 2012; 11: 150-6.
43. Baron F, Lechanteur C, Willems E, Bruck F, Baudoux E, Seidel L, et al. Cotransplantation of mesenchymal stem cells might prevent death from graft-versus-host disease (GVHD) without abrogating graft-versus-tumor effects after HLA-mismatched allogeneic transplantation following nonmyeloablative conditioning. Biology of blood and marrow transplantation: journal of the American Society for Blood and Marrow Transplantation. 2010; 16: 838.
44. Hare JM, Fishman JE, Gerstenblith G, Velazquez DLDF, Zambrano JP, Suncion VY, et al. Comparison of Allogeneic vs Autologous Bone Marrow-Derived Mesenchymal Stem Cells Delivered by Transendocardial Injection in Patients With Ischemic CardiomyopathyThe POSEIDON Randomized TrialMesenchymal Stem Cells and Ischemic Cardiomyopathy. JAMA: The Journal of the American Medical Association. 2012; 308: 2369-79.
45. Hare JM, Traverse JH, Henry TD, Dib N, Strumpf RK, Schulman SP, et al. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. Journal of the American College of Cardiology. 2009; 54: 2277-86.
46. Tan J, Wu W, Xu X, Liao L, Zheng F, Messinger S, et al. Induction Therapy With Autologous Mesenchymal Stem Cells in Living-Related Kidney Transplants A Randomized Controlled Trial. JAMA: The Journal of the American Medical Association. 2012; 307: 1169-77.
47. Reinders ME, de Fijter JW, Roelofs H, Bajema IM, de Vries DK, Schaapherder AF, et al. Autologous bone marrow-derived mesenchymal stromal cells for the treatment of allograft rejection after renal transplantation: results of a phase I study. Stem cells translational medicine. 2013; 2: 107-11.
48. Gupta PK, Chullikana A, Parakh R, Desai S, Das A, Gottipamula S, et al. 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. 2013; 11: 143.
49. Lee SH, Lee MW, Yoo KH, Kim DS, Son MH, Sung KW, et al. Co-transplantation of third-party umbilical cord blood-derived MSCs promotes engraftment in children undergoing unrelated umbilical cord blood transplantation. Bone marrow transplantation. 2013; 48: 1040-5.
50. Lee PH, Lee JE, Kim HS, Song SK, Lee HS, Nam HS, et al. A randomized trial of mesenchymal stem cells in multiple system atrophy. Ann Neurol. 2012; 72: 32-40.
51. Ra JC, Shin IS, Kim SH, Kang SK, Kang BC, Lee HY, et al. Safety of intravenous infusion of human adipose tissue-derived mesenchymal stem cells in animals and humans. Stem Cells Dev. 2011; 20: 1297-308.
52. Weiss DJ, Casaburi R, Flannery R, LeRoux-Williams M, Tashkin DP. A placebo-controlled, randomized trial of mesenchymal stem cells in COPD. Chest. 2013; 143: 1590-8.
53. Peng L, Xie DY, Lin BL, Liu J, Zhu HP, Xie C, et al. Autologous bone marrow mesenchymal stem cell transplantation in liver failure patients caused by hepatitis B: short-term and long-term outcomes. Hepatology. 2011; 54: 820-8.
54. Otsuru S, Gordon PL, Shimono K, Jethva R, Marino R, Phillips CL, et al. Transplanted bone marrow mononuclear cells and MSCs impart clinical benefit to children with osteogenesis imperfecta through different mechanisms. Blood. 2012; 120: 1933-41.
55. El-Kheir WA, Gabr H, Awad MR, Ghannam O, Barakat Y, Farghali HA, et al. Autologous bone marrow-derived cell therapy combined with physical therapy induces functional improvement in chronic spinal cord injury patients. Cell transplantation. 2013.
56. Shahdadfar A, Frønsdal K, Haug T, Reinholt FP, Brinchmann JE. In vitro expansion of human mesenchymal stem cells: choice of serum is a determinant of cell proliferation, differentiation, gene expression, and transcriptome stability. Stem cells. 2005; 23: 1357-66.
57. Mohyeldin A, Garzón-Muvdi T, Quiñones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell stem cell. 2010; 7: 150.
58. Gebler A, Zabel O, Seliger B. The immunomodulatory capacity of mesenchymal stem cells. Trends Mol Med. 2012; 18: 128-34.
59. Plock JA, Schnider JT, Solari MG, Zheng XX, Gorantla VS. Perspectives on the use of mesenchymal stem cells in vascularized composite allotransplantation. Frontiers in immunology. 2013; 4: 175.
60. Francois M, Romieu-Mourez R, Li M, Galipeau J. Human MSC suppression correlates with cytokine induction of indoleamine 2,3-dioxygenase and bystander M2 macrophage differentiation. Molecular therapy : the journal of the American Society of Gene Therapy. 2012; 20: 187-95.
61. Klyushnenkova E, Mosca JD, Zernetkina V, Majumdar MK, Beggs KJ, Simonetti DW, et al. T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression. J Biomed Sci. 2005; 12: 47-57.
62. Ankrum JA, Ong JF, Karp JM. Mesenchymal stem cells: immune evasive, not immune privileged. Nat Biotechnol. 2014; 32: 252-60.
63. Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Experimental hematology. 2003; 31: 890-6.
64. Spees JL, Gregory CA, Singh H, Tucker HA, Peister A, Lynch PJ, et al. Internalized Antigens Must Be Removed to Prepare Hypoimmunogenic Mesenchymal Stem Cells for Cell and Gene Therapy&ast. Molecular Therapy. 2004; 9: 747-56.
65. 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. 2006; 25: 197-202.
66. Komoda H, Okura H, Lee C, Sougawa N, Iwayama T, Hashikawa T, et al. Reduction of N-glycolylneuraminic acid xenoantigen on human adipose tissue-derived stromal cells/mesenchymal stem cells leads to safer and more useful cell sources for various stem cell therapies. Tissue engineering Part A. 2010; 16: 1143.
67. Ghaderi D, Taylor RE, Padler-Karavani V, DiazS, Varki A. Implications of the presence of N-glycolylneuraminic acid in recombinant therapeutic glycoproteins. Nat Biotechnol. 2010; 28: 863-7.
68. Zhu A, Hurst R. Anti-N-glycolylneuraminic acid antibodies identified in healthy human serum. Xenotransplantation. 2002; 9: 376-81.
69. Li Y, Lin F. Mesenchymal stem cells are injured by complement after their contact with serum. Blood. 2012; 120: 3436-43.
70. Tu Z, Li Q, Bu H, Lin F. Mesenchymal stem cells inhibit complement activation by secreting factor H. Stem Cells Dev. 2010; 19: 1803-9.
71. Padler-Karavani V, Varki A. Potential impact of the non‐human sialic acid N‐glycolylneuraminic acid on transplant rejection risk. Xenotransplantation. 2011; 18: 1-5.
72. Dedrick V. Determining the safety of medical devices containing animal tissue: the new European standards. J Regul Affairs Prof Soc. 1997; 4: 2-20.
73. Cobo F, Talavera P, Concha A. Diagnostic approaches for viruses and prions in stem cell banks. Virology. 2006; 347: 1-10.
74. Lepperdinger G, Brunauer R, Jamnig A, Laschober G, Kassem M. Controversial issue: Is it safe to employ mesenchymal stem cells in cell-based therapies? Experimental Gerontology. 2008; 43: 1018-23.
75. Bonab MM, Alimoghaddam K, Talebian F, Ghaffari SH, Ghavamzadeh A, Nikbin B. Aging of mesenchymal stem cell in vitro. BMC cell biology. 2006; 7: 14.
76. Wagner W, Horn P, Castoldi M, Diehlmann A, Bork S, Saffrich R, et al. Replicative senescence of mesenchymal stem cells: a continuous and organized process. PloS one. 2008; 3: e2213.
77. Schellenberg A, Lin Q, Schüler H, Koch CM, Joussen S, Denecke B, et al. Replicative senescence of mesenchymal stem cells causes DNA-methylation changes which correlate with repressive histone marks. Aging (Albany NY). 2011; 3: 873.
78. Collado M, Blasco MA, Serrano M. Cellular Senescence in Cancer and Aging. Cell. 2007; 130: 223-33.
79. Kuilman T, Michaloglou C, Mooi WJ, Peeper DS. The essence of senescence. Genes & development. 2010; 24: 2463-79.
80. Ho JH, Chen YF, Ma WH, Tseng TC, Chen MH, Lee OK. Cell contact accelerates replicative senescence of human mesenchymal stem cells independent of telomere shortening and p53 activation: roles of Ras and oxidative stress. Cell transplantation. 2011; 20: 1209-20.
81. Hiyama E, Hiyama K. Telomere and telomerase in stem cells. Br J Cancer. 2007; 96: 1020-4.
82. Fehrer C, Lepperdinger G. Mesenchymal stem cell aging. Experimental Gerontology. 2005; 40: 926-30.
83. Yanada S, Ochi M, Kojima K, Sharman P, Yasunaga Y, Hiyama E. Possibility of selection of chondrogenic progenitor cells by telomere length in FGF-2-expanded mesenchymal stromal cells. Cell Proliferation. 2006; 39: 575-84.
84. Bianchi G, Banfi A, Mastrogiacomo M, Notaro R, Luzzatto L, Cancedda R, et al. Ex vivo enrichment of mesenchymal cell progenitors by fibroblast growth factor 2. Experimental Cell Research. 2003; 287: 98-105.
85. Handorf AM, Li W-J. Fibroblast Growth Factor-2 Primes Human Mesenchymal Stem Cells for Enhanced Chondrogenesis. PLoS ONE. 2011; 6: e22887.
86. Choo KB, Tai L, Hymavathee KS, Wong CY, Nguyen PNN, Huang C-J, et al. Oxidative Stress-Induced Premature Senescence in Wharton's Jelly-Derived Mesenchymal Stem Cells. International journal of medical sciences. 2014; 11: 1201.
87. Limb GA, Daniels JT. Ocular regeneration by stem cells: present status and future prospects. British medical bulletin. 2008; 85: 47-61.
88. Song CH, Honmou O, Furuoka H, Horiuchi M. Identification of chemoattractive factors involved in the migration of bone marrow-derived mesenchymal stem cells to brain lesions caused by prions. Journal of virology. 2011; 85: 11069-78.
89. Wu Y, Zhao RCH. The role of chemokines in mesenchymal stem cell homing to myocardium. Stem Cell Reviews and Reports. 2012; 8: 243-50.
90. Ponte AL, Marais E, Gallay N, Langonne A, Delorme B, Herault O, et al. The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells. 2007; 25: 1737-45.
91. Smith H, Whittall C, Weksler B, Middleton J. Chemokines stimulate bidirectional migration of human mesenchymal stem cells across bone marrow endothelial cells. Stem Cells Dev. 2012; 21: 476-86.
92. Baek SJ, Kang SK, Ra JC. In vitro migration capacity of human adipose tissue-derived mesenchymal stem cells reflects their expression of receptors for chemokines and growth factors. Exp Mol Med. 2011; 43: 596-603.
93. Honczarenko M, Le Y, Swierkowski M, Ghiran I, Glodek AM, Silberstein LE. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells. 2006; 24: 1030-41.
94. Fiedler J, Brill C, Blum WF, Brenner RE. IGF-I and IGF-II stimulate directed cell migration of bone-marrow-derived human mesenchymal progenitor cells. Biochemical and biophysical research communications. 2006; 345: 1177-83.
95. 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.
96. Tamama K, Fan VH, Griffith LG, Blair HC, Wells A. Epidermal growth factor as a candidate for ex vivo expansion of bone marrow-derived mesenchymal stem cells. Stem cells. 2006; 24: 686-95.
97. Phipps MC, Xu Y, Bellis SL. Delivery of platelet-derived growth factor as a chemotactic factor for mesenchymal stem cells by bone-mimetic electrospun scaffolds. PloS one. 2012; 7: e40831.
98. Whitford WG. Supplementation of animal cell culture media. BioProcess Int. 2005; 3.
99. Gstraunthaler G. Alternatives to the use of fetal bovine serum: serum-free cell culture. Altex. 2003; 20: 275-81.
100. Lindroos B, Boucher S, Chase L, Kuokkanen H, Huhtala H, Haataja R, et al. Serum-free, xeno-free culture media maintain the proliferation rate and multipotentiality of adipose stem cells in vitro. Cytotherapy. 2009; 11: 958-72.
101. 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: 1436-46.
102. Simoes IN, Boura JS, dos Santos F, Andrade PZ, Cardoso CM, Gimble JM, et al. Human mesenchymal stem cells from the umbilical cord matrix: successful isolation and ex vivo expansion using serum-/xeno-free culture media. Biotechnology journal. 2013; 8: 448-58.
103. Corotchi MC, Popa MA, Remes A, Sima LE, Gussi I, Plesu M. Isolation method and xeno-free culture conditions influence multipotent differentiation capacity of human Wharton’s jelly-derived mesenchymal stem cells. Stem Cell Res Ther. 2013; 4: 81.
104. Patrikoski M, Juntunen M, Boucher S, Campbell A, Vemuri MC, Mannerström B, et al. Development of fully defined xeno-free culture system for the preparation and propagation of cell therapy-compliant human adipose stem cells. Stem cell research & therapy. 2013; 4: 27.
105. Chase LG, Lakshmipathy U, Solchaga LA, Rao MS, Vemuri MC. A novel serum-free medium for the expansion of human mesenchymal stem cells. Stem Cell Res Ther. 2010; 1: 1549-53.
106. Rashi K-J. Growth and Differentiation of Human Dental Pulp Stem Cells Maintained in Fetal Bovine Serum, Human Serum and Serum-free/Xeno-free Culture Media. Journal of Stem Cell Research & Therapy. 2012; 2: 4.
107. Crapnell K, Blaesius R, Hastings A, Lennon DP, Bruder SP. Growth, Differentiation Capacity, and Function of Mesenchymal Stem Cells Expanded in Serum-Free Medium Developed Via Combinatorial Screening. Experimental cell research. 2013; 319: 1409-18.
108. Aldahmash A, Haack-Sorensen M, Al-Nbaheen M, Harkness L, Abdallah BM, Kassem M. Human Serum is as Efficient as Fetal Bovine Serum in Supporting Proliferation and Differentiation of Human Multipotent Stromal (Mesenchymal) Stem Cells In Vitro and In Vivo. Stem Cell Reviews and Reports. 2011; 7: 860-8.
109. Lin HT, Tarng YW, Chen YC, Kao CL, Hsu CJ, Shyr YM, et al. Using Human Plasma Supplemented Medium to Cultivate Human Bone Marrow-Derived Mesenchymal Stem Cell and Evaluation of Its Multiple-Lineage Potential. Transplantation proceedings: Elsevier; 2005: 4504-5.
110. Jonsdottir-Buch SM, Lieder R, Sigurjonsson OE. Platelet lysates produced from expired platelet concentrates support growth and osteogenic differentiation of mesenchymal stem cells. PLoS One. 2013; 8: e68984.
111. Stute N, Holtz K, Bubenheim M, Lange C, Blake F, Zander AR. Autologous serum for isolation and expansion of human mesenchymal stem cells for clinical use. Experimental hematology. 2004; 32: 1212-25.
112. 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 biology international. 2006; 30: 521-4.
113. 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: 1901-10.
114. Kobayashi T, Watanabe H, Yanagawa T, Tsutsumi S, Kayakabe M, Shinozaki T, et al. Motility and growth of human bone-marrow mesenchymal stem cells during ex vivo expansion in autologous serum. Journal of Bone & Joint Surgery, British Volume. 2005; 87: 1426-33.
115. Dahl J-A, Duggal S, Coulston N, Millar D, Melki J, Shandadfar A, et al. Genetic and epigenetic instability of human bone marrow mesenchymal stem cells expanded in autologous serum or fetal bovine serum. International Journal of Developmental Biology. 2008; 52: 1033.
116. Jung S, Panchalingam KM, Rosenberg L, Behie LA. Ex Vivo Expansion of Human Mesenchymal Stem Cells in Defined Serum-Free Media. Stem Cells International. 2012; 2012: 21.
117. Cooper K, SenMajumdar A, Viswanathan C. Derivation, expansion and characterization of clinical grade mesenchymal stem cells from umbilical cord matrix using cord blood serum. International journal of stem cells. 2010; 3: 119.
118. Jung J, Moon N, Ahn JY, Oh EJ, Kim M, Cho CS, et al. Mesenchymal stromal cells expanded in human allogenic cord blood serum display higher self-renewal and enhanced osteogenic potential. Stem cells and development. 2009; 18: 559-72.
119. Bieback K, Hecker A, Schlechter T, Hofmann I, Brousos N, Redmer T, et al. Replicative aging and differentiation potential of human adipose tissue-derived mesenchymal stromal cells expanded in pooled human or fetal bovine serum. Cytotherapy. 2012; 14: 570-83.
120. Turnovcova K, Ruzickova K, Vanecek V, Sykova E, Jendelova P. Properties and growth of human bone marrow mesenchymal stromal cells cultivated in different media. Cytotherapy. 2009; 11: 874-85.
121. Tateishi K, Ando W, Higuchi C, Hart D, Hashimoto J, Nakata K, et al. Comparison of human serum with fetal bovine serum for expansion and differentiation of human synovial MSC: potential feasibility for clinical applications. Cell transplantation. 2008; 17: 549-57.
122. Le Blanc K, Samuelsson H, Lönnies L, Sundin M, Ringdén O. Generation of immunosuppressive mesenchymal stem cells in allogeneic human serum. Transplantation. 2007; 84: 1055-9.
123. Poloni A, Maurizi G, Rosini V, Mondini E, Mancini S, Discepoli G, et al. Selection of CD271+ cells and human AB serum allows a large expansion of mesenchymal stromal cells from human bone marrow. Cytotherapy. 2009; 11: 153-62.
124. Phadnis SM, Joglekar MV, Venkateshan V, Ghaskadbi SM, Hardikar AA, Bhonde RR. Human umbilical cord blood serum promotes growth, proliferation, as well as differentiation of human bone marrow-derived progenitor cells. In vitro cellular & developmental biology Animal. 2006; 42: 283-6.
125. Crespo-Diaz R, Behfar A, Butler GW, Padley DJ, Sarr MG, Bartunek J, et al. Platelet lysate consisting of a natural repair proteome supports human mesenchymal stem cell proliferation and chromosomal stability. Cell transplantation. 2011; 20: 797-811.
126. Griffiths S, Baraniak PR, Copland IB, Nerem RM, McDevitt TC. Human platelet lysate stimulates high-passage and senescent human multipotent mesenchymal stromal cell growth and rejuvenation in vitro. Cytotherapy. 2013; 15: 1469-83.
127. Trojahn Kolle SF, Oliveri RS, Glovinski PV, Kirchhoff M, Mathiasen AB, Elberg JJ, et al. Pooled human platelet lysate versus fetal bovine serum-investigating the proliferation rate, chromosome stability and angiogenic potential of human adipose tissue-derived stem cells intended for clinical use. Cytotherapy. 2013; 15: 1086-97.
128. 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 transplantation. 2007; 40: 785-91.
129. Govindasamy V, Ronald VS, Abdullah ANB, Ganesan Nathan KR, Aziz ZACA, Abdullah M, et al. Human platelet lysate permits scale-up of dental pulp stromal cells for clinical applications. Cytotherapy. 2011; 13: 1221-33.
130. Vasanthan P, Gnanasegaran N, Govindasamy V, Abdullah AN, Jayaraman P, Ronald VS, et al. Comparison of fetal bovine serum and human platelet lysate in cultivation and differentiation of dental pulp stem cells into hepatic lineage cells. Biochemical Engineering Journal. 2014; 88: 142-53.
131. Vunjak-Novakovic G, Scadden DT. Biomimetic platforms for human stem cell research. Cell stem cell. 2011; 8: 252-61.
132. Wagers AJ. The Stem Cell Niche in Regenerative Medicine. Cell stem cell. 2012; 10: 362-9.
133. Fiedler J, Roderer G, Gunther KP, Brenner RE. BMP-2, BMP-4, and PDGF-bb stimulate chemotactic migration of primary human mesenchymal progenitor cells. J Cell Biochem. 2002; 87: 305-12.
134. Ji JF, He BP, Dheen ST, Tay SS. Interactions of chemokines and chemokine receptors mediate the migration of mesenchymal stem cells to the impaired site in the brain after hypoglossal nerve injury. Stem Cells. 2004; 22: 415-27.
135. Aliotta JM, Pereira M, Johnson KW, de Paz N, Dooner MS, Puente N, et al. Microvesicle entry into marrow cells mediates tissue-specific changes in mRNA by direct delivery of mRNA and induction of transcription. Experimental hematology. 2010; 38: 233-45.
136. Ratajczak M, Kucia M, Jadczyk T, Greco N, Wojakowski W, Tendera M, et al. Pivotal role of paracrine effects in stem cell therapies in regenerative medicine: can we translate stem cell-secreted paracrine factors and microvesicles into better therapeutic strategies&quest. Leukemia. 2012; 26: 1166-73.
137. Sabin K, Kikyo N. Microvesicles as mediators of tissue regeneration. Translational research : the journal of laboratory and clinical medicine. 2014; 163: 286-95.
138. Yuan A, Farber EL, Rapoport AL, Tejada D, Deniskin R, Akhmedov NB, et al. Transfer of MicroRNAs by Embryonic Stem Cell Microvesicles. PLoS ONE. 2009; 4: e4722.
139. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia. 2006; 20: 847-56.
140. Rozmyslowicz T, Majka M, Kijowski J, Murphy SL, Conover DO, Poncz M, et al. Platelet-and megakaryocyte-derived microparticles transfer CXCR4 receptor to CXCR4-null cells and make them susceptible to infection by X4-HIV. AIDS (London, England). 2003; 17: 33-42.
141. Biancone L, Bruno S, Deregibus MC, Tetta C, Camussi G. Therapeutic potential of mesenchymal stem cell-derived microvesicles. Nephrology Dialysis Transplantation. 2012; 27: 3037-42.
142. Camussi G, Deregibus MC, Bruno S, Cantaluppi V, Biancone L. Exosomes?microvesicles as a mechanism of cell-to-cell communication. Kidney Int. 2010; 78: 838-48.
143. Mrvar-Brečko A, Šuštar V, Janša V, Štukelj R, Janša R, Mujagić E, et al. Isolated microvesicles from peripheral blood and body fluids as observed by scanning electron microscope. Blood Cells, Molecules, and Diseases. 2010; 44: 307-12.
144. Quesenberry PJ, Dooner MS, Aliotta JM. Stem cell plasticity revisited: the continuum marrow model and phenotypic changes mediated by microvesicles. Experimental hematology. 2010; 38: 581-92.
145. Deregibus MC, Cantaluppi V, Calogero R, Lo Iacono M, Tetta C, Biancone L, et al. Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood. 2007; 110: 2440-8.
146. Lee Y, Andaloussi SE, Wood MJ. Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Human molecular genetics. 2012; 21: R125-R34.
147. Ripa RS, Wang Y, Goetze JP, Jørgensen E, Johnsen HE, Tägil K, et al. Circulating angiogenic cytokines and stem cells in patients with severe chronic ischemic heart disease—Indicators of myocardial ischemic burden? International journal of cardiology. 2007; 120: 181-7.
148. Ferrarese C, Mascarucci P, Zoia C, Cavarretta R, Frigo M, Begni B, et al. Increased cytokine release from peripheral blood cells after acute stroke. Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism. 1999; 19: 1004-9.
149. Intiso D, Zarrelli MM, Lagioia G, Di Rienzo F, Checchia De Ambrosio C, Simone P, et al. Tumor necrosis factor alpha serum levels and inflammatory response in acute ischemic stroke patients. Neurological sciences : official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology. 2004; 24: 390-6.
150. Drimal J, Knezl V, Paulovicova E, Drimal D. Enhanced early after-myocardial infarction concentration of TNF-alpha subsequently increased circulating and myocardial adrenomedullin in spontaneously hypertensive rats. General physiology and biophysics. 2008; 27: 12-8.
151. Lionetti V, Bianchi G, Recchia FA, Ventura C. Control of autocrine and paracrine myocardial signals: an emerging therapeutic strategy in heart failure. Heart failure reviews. 2010; 15: 531-42.
152. Harrison JS, Rameshwar P, Chang V, Bandari P. Oxygen saturation in the bone marrow of healthy volunteers. Blood. 2002; 99: 394.
153. Panchision DM. The role of oxygen in regulating neural stem cells in development and disease. Journal of cellular physiology. 2009; 220: 562-8.
154. Eliasson P, Jönsson JI. The hematopoietic stem cell niche: low in oxygen but a nice place to be. Journal of cellular physiology. 2010; 222: 17-22.