Potential for neural differentiation of mesenchymal stem cells

Advances in Biochemical Engineering/Biotechnology

Volumn 129, Issue , 2013, Pages 89-115

  Ferroni, Letizia ^a   Gardin, Chiara ^a   Tocco Tussardi, Ilaria ^a   Epis, Roberta ^b   Casadei, Alessandro ^c   Vindigni, Vincenzo ^a   Mucci, Giuseppe ^b   Zavan, Barbara ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b Bioscience Institute   (Italy)

^c Private Practice of Plastic Surgery (Board certified)   (Italy)

Author keywords

Adipose derived stem cells; Clinical application; MSC; Neuronal commitment

Indexed keywords

ADIPOSE TISSUE; ANIMAL; ARTICLE; CELL DIFFERENTIATION; CYTOLOGY; HUMAN; MESENCHYMAL STROMA CELL; METHODOLOGY; NERVE CELL; NEURAL STEM CELL; PHYSIOLOGY; REGENERATIVE MEDICINE; STEM CELL;

ADIPOSE TISSUE; ANIMALS; CELL DIFFERENTIATION; HUMANS; MESENCHYMAL STROMAL CELLS; NEURAL STEM CELLS; NEURONS; REGENERATIVE MEDICINE; STEM CELLS;

EID: 84882932250     PISSN: 07246145     EISSN: None     Source Type: Book Series    
DOI: 10.1007/10_2012_152     Document Type: Article

References (112)

1. Aguiari P, Leo S, Zavan B et al (2008) High glucose induces adipogenic differentiation of muscle-derived stem cells. Proc Natl Acad Sci U SA 105:1226-1231
2. Ahrens N, Tormin A, Paulus M et al (2004) Mesenchymal stem cell content of human vertebral bone marrow. Transplantation 78:925-929
3. Al Battah F, De Kock J, Vanhaecke T et al (2011) Current status of human adipose-derived stem cells: differentiation into hepatocyte-like cells. ScientificWorldJournal 11:1568-1581
4. Amos PJ, Kapur SK, Stapor PC et al (2010) Human adipose-derived stromal cells accelerate diabetic wound healing: impact of cell formulation and delivery. Tissue Eng Part A 16:1595-1606
5. Arboleda D, Forostyak S, Jendelova P et al (2011) Transplantation of predifferentiated adipose-derived stromal cells for the treatment of spinal cord injury. Cell Mol Neurobiol 31:1113-1122
6. Arrigoni E, Lopa S, de Girolamo L et al (2009) Isolation, characterization and osteogenic differentiation of adipose-derived stem cells: from small to large animal models. Cell Tissue Res 338:401-411
7. Aust L, Devlin B, Foster SJ et al (2004) Yield of human adipose-derived adult stem cells from liposuction aspirates. Cytotherapy 6:7-14
8. Aziz A, Miyake T, Engleka KA et al (2009) Menin expression modulates mesenchymal cell commitment to the myogenic and osteogenic lineages. Dev Biol 332:116-130
9. Bailey AM, Kapur S, Katz AJ (2010) Characterization of adipose-derived stem cells: an update. Curr Stem Cell Res Ther 5:95-102
10. Banerjee M, Bhonde RR (2006) Application of hanging drop technique for stem cell differentiation and cytotoxicity studies. Cytotechnology 51:1-5
11. Belicchi M, Pisati F, Lopa R et al (2004) Human skin-derived stem cells migrate throughout forebrain and differentiate into astrocytes after injection into adult mouse brain. J Neurosci Res 77:475-486
12. Bieback K, Hecker A, Kocaömer A et al (2009) Human alternatives to fetal bovine serum for the expansion of mesenchymal stromal cells from bone marrow. Stem Cells 27:2331-2341
13. Bieback K, Kinzebach S, Karagianni M (2011) Translating research into clinical scale manufacturing of mesenchymal stromal cells. Stem Cells Int 2010:193519
14. Blande IS, Bassaneze V, Lavini-Ramos C et al (2009) Adipose tissue mesenchymal stem cell expansion in animal serum-free medium supplemented with autologous human platelet lysate. Transfusion 49:2680-2685
15. Bruder SP, Jaiswal N, Haynesworth SE (1997) Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J Cell Biochem 64:278-294
16. Caplan AI (1991) Mesenchymal stem cells. J Orthop Res 9:641-650
17. Carpenter MK, Inokuma MS, Denham J et al (2001) Enrichment of neurons and neural precursors from human embryonic stem cells. Exp Neurol 172:383-397
18. Casteilla L, Planat-Bénard V, Cousin B et al (2005) Plasticity of adipose tissue: a promising therapeutic avenue in the treatment of cardiovascular and blood diseases? Arch Mal Coeur Vaiss 98:922-926
19. Chen J, Li Y, Wang L, Zhang Z et al (2001) Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 32:1005-1011
20. Chen J, Li Y, Katakowski M et al (2003) Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J Neurosci Res 73:778-786
21. Chen X, Li Y, Wang L et al (2002) Ischemic rat brain extracts induce human marrow stromal cell growth factor production. Neuropathology 22:275-279
22. Chi GF, Kim MR, Kim DW et al (2010) Schwann cells differentiated from spheroid-forming cells of rat subcutaneous fat tissue myelinate axons in the spinal cord injury. Exp Neurol 222:304-317
23. Choi YS, Noh SE, Lim SM et al (2008) Multipotency and growth characteristic of periosteum-derived progenitor cells for chondrogenic, osteogenic, and adipogenic differentiation. Biotechnol Lett 30:593-601
24. Cízková D, Rosocha J, VanickýI et al (2006) Transplants of human mesenchymal stem cells improve functional recovery after spinal cord injury in the rat. Cell Mol Neurobiol 26:1167-1180
25. da Justa Pinheiro CH, de Queiroz JC, Guimarães-Ferreira L et al (2011) Local injections of adipose-derived mesenchymal stem cells modulate inflammation and increase angiogenesis ameliorating the dystrophic phenotype in dystrophin-deficient skeletal muscle. Stem Cell Rev 8(2):363-374 (Epub ahead of print)
26. De Bari C, Dell'Accio F, Tylzanowski P et al (2001) Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 44:1928-1942
27. Dodson MV, Hausman GJ, Guan L et al (2010) Skeletal muscle stem cells from animals I. Basic cell biology. Int J Biol Sci 6:465-474
28. Dominici M, Le Blanc K, Mueller I et al (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315-317
29. Elabd C, Chiellini C, Carmona M et al (2009) Human multipotent adipose-derived stem cells differentiate into functional brown adipocytes. Stem Cells 27:2753-2760
30. Faulkner J, Keirstead HS (2005) Human embryonic stem cell-derived oligodendrocyte progenitors for the treatment of spinal cord injury. Transpl Immunol 15:131-142
31. Feng J, Mantesso A, Sharpe PT (2010) Perivascular cells as mesenchymal stem cells. Expert Opin Biol Ther 10:1441-1451
32. Fernandes KJ, Kobayashi NR, Gallagher CJ et al (2006) Analysis of the neurogenic potential of multipotent skin-derived precursors. Exp Neurol 201:32-48
33. Ferreira A, Caceres A (1992) Expression of the class III beta-tubulin isotype in developing neurons in culture. J Neurosci Res 32:516-529
34. Fink T, Rasmussen JG, Lund P et al (2011) Isolation and expansion of adipose-derived stem cells for tissue engineering. Front Biosci (Elite Ed) 3:256-263
35. Franco Lambert AP, Fraga Zandonai A, Bonatto D et al (2009) Differentiation of human adipose-derived adult stem cells into neuronal tissue: does it work? Differentiation 77:221-228
36. Freyberg S, Song YH, Muehlberg F et al (2009) Thrombin peptide (TP508) promotes adipose tissue-derived stem cell proliferation via PI3 kinase/Akt pathway. J Vasc Res 46:98-102
37. Gao J, Dennis JE, Muzic RF et al (2001) The dynamic in vivo distribution of bone marrowderived mesenchymal stem cells after infusion. Cells Tissues Organs 169:12-20
38. Gimble JM, Katz AJ, Bunnell BA (2007) Adipose-derived stem cells for regenerative medicine. Circ Res 100:1249-1260
39. Gimble JM, Guilak F, Nuttall ME et al (2008) In vitro differentiation potential of mesenchymal stem cells. Transfus Med Hemother 35:228-238
40. Gimble JM, Bunnell BA, Chiu ES et al (2011) Concise review: Adipose-derived stromal vascular fraction cells and stem cells: let's not get lost in translation. Stem Cells 29:749-754
41. Gruber HE, Somayaji S, Riley F et al (2012) Human adipose-derived mesenchymal stem cells: serial passaging, doubling time and cell senescence. Biotech Histochem 87:303-311
42. Guilak F, Lott KE, Awad HA et al (2006) Clonal analysis of the differentiation potential of human adipose-derived adult stem cells. J Cell Physiol 206:229-237
43. Hicok KC, Du Laney TV, Zhou YS et al (2004) Human adipose-derived adult stem cells produce osteoid in vivo. Tissue Eng 10:371-380
44. Izadpanah R, Trygg C, Patel B et al (2006) Biologic properties of mesenchymal stem cells derived from bone marrow and adipose tissue. J Cell Biochem 99:1285-1297
45. Jeon BG, Kumar BM, Kang EJ et al (2011) Characterization and comparison of telomere length, telomerase and reverse transcriptase activity and gene expression in human mesenchymal stem cells and cancer cells of various origins. Cell Tissue Res 345:149-161
46. Kakudo N, Minakata T, Mitsui T et al (2008) Proliferation-promoting effect of platelet-rich plasma on human adipose-derived stem cells and human dermal fibroblasts. Plast Reconstr Surg 122:1352-1360
47. Kang SK, Lee DH, Bae YC et al (2003) Improvement of neurological deficits by intracerebral transplantation of human adipose tissue-derived stromal cells after cerebral ischemia in rats. Exp Neurol 183:355-366
48. Kang YJ, Jeon ES, Song HY et al (2005) Role of c-Jun N-terminal kinase in the PDGFinduced proliferation and migration of human adipose tissue-derived mesenchymal stem cells. J Cell Biochem 95:1135-1145
49. Katz AJ, Tholpady A, Tholpady SS et al (2005) Cell surface and transcriptional characterization of human adipose-derived adherent stromal (hADAS) cells. Stem Cells 23:412-423
50. Kim HJ, Im GI (2009) Combination of transforming growth factor-beta2 and bone morphogenetic protein 7 enhances chondrogenesis from adipose tissue-derived mesenchymal stem cells. Tissue Eng Part A 15:1543-1551
51. Kim JM, Lee ST, Chu K et al (2007) Systemic transplantation of human adipose stem cells attenuated cerebral inflammation and degeneration in a hemorrhagic stroke model. Brain Res 1183:43-50
52. Knippenberg M, Helder MN, Doulabi BZ et al (2005) Adipose tissue-derived mesenchymal stem cells acquire bone cell-like responsiveness to fluid shear stress on osteogenic stimulation. Tissue Eng 11:1780-1788
53. Kocaoemer A, Kern S, Klüter H et al (2007) 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 25:1270-1278
54. Kozlov G, Lee J, Elias D, Gravel M et al (2003) Structural evidence that brain cyclic nucleotide phosphodiesterase is a member of the 2H phosphodiesterase superfamily. J Biol Chem 278(46):46021-46028
55. Kubal WS (2012) Updated imaging of traumatic brain injury. Radiol Clin North Am 50:15-41
56. Kulikov AV, Stepanova MS, Stvolinsky SL (2008) Application of multipotent mesenchymal stromal cells from human adipose tissue for compensation of neurological deficiency induced by 3-nitropropionic Acid in rats. Bull Exp Biol Med 145:514-519
57. Lee J, Gravel M, Zhang R et al (2005) Process outgrowth in oligodendrocytes is mediated by CNP, a novel microtubule assembly myelin protein. J Cell Biol 170:661-673
58. Li Y, Chopp M, Chen J et al (2000) Intrastriatal transplantation of bone marrow nonhematopoietic cells improves functional recovery after stroke in adult mice. J Cereb Blood Flow Metab 20:1311-1319
59. Lindroos B, Suuronen R, Miettinen S (2011) The potential of adipose stem cells in regenerative medicine. Stem Cell Rev 7:269-291
60. Lindvall O, Kokaia Z (2010) Stem cells in human neurodegenerative disorders-time for clinical translation? J Clin Invest 120:29-40
61. Lo EH, Dalkara T, Moskowitz MA (2003) Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 4:399-415
62. Locke M, Feisst V, Dunbar PR (2011) Concise review: human adipose-derived stem cells: separating promise from clinical need. Stem Cells 29:404-411
63. Lu D, Sanberg PR, Mahmood A et al (2002) Intravenous administration of human umbilical cord blood reduces neurological deficit in the rat after traumatic brain injury. Cell Transplant 11:275-281
64. Madonna R, Renna FV, Cellini C et al (2011) Age-dependent impairment of number and angiogenic potential of adipose tissue-derived progenitor cells. Eur J Clin Invest 41:126-133
65. Mahmood A, Lu D, Lu M et al (2003) Treatment of traumatic brain injury in adult rats with intravenous administration of human bone marrow stromal cells. Neurosurgery 53:697-702
66. Michalczyk K, Ziman M (2005) Nestin structure and predicted function in cellular cytoskeletal organisation. Histol Histopathol 20:665-671
67. Mitchell JB, McIntosh K, Zvonic S et al (2006) Immunophenotype of human adiposederived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem Cells 24:376-385
68. Miura M, Gronthos S, Zhao M et al (2003) SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A 100:5807-5812
69. Mojallal A, Lequeux C, Shipkov C et al (2011) Influence of age and body mass index on the yield and proliferation capacity of adipose-derived stem cells. Aesthetic Plast Surg 35:1097-1105
70. Oedayrajsingh-Varma MJ, van Ham SM, Knippenberg M et al (2006) Adipose tissuederived mesenchymal stem cell yield and growth characteristics are affected by the tissueharvesting procedure. Cytotherapy 8:166-177
71. Ogawa R, Mizuno H, Watanabe A et al (2004) Osteogenic and chondrogenic differentiation by adipose-derived stem cells harvested from GFP transgenic mice. Biochem Biophys Res Commun 313:871-877
72. Onda T, Honmou O, Harada K (2008) Therapeutic benefits by human mesenchymal stem cells (hMSCs) and Ang-1 gene-modified hMSCs after cerebral ischemia. J Cereb Blood Flow Metab 28:329-340
73. Pittenger MF, Mackay AM, Beck SC et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147
74. Planat-Bénard V, Menard C, AndréMet al (2004) Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circ Res 94:223-229
75. Puissant B, Barreau C, Bourin P et al (2005) Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol 129:118-129
76. Rodriguez AM, Elabd C, Amri EZ et al (2005) The human adipose tissue is a source of multipotent stem cells. Biochimie 87:125-128
77. Romanov YA, Darevskaya AN, Merzlikina NV et al (2005) Mesenchymal stem cells from human bone marrow and adipose tissue: isolation, characterization, and differentiation potentialities. Bull Exp Biol Med 140:138-143
78. Rowland JW, Hawryluk GW, Kwon B et al (2008) Current status of acute spinal cord injury pathophysiology and emerging therapies: promise on the horizon. Neurosurg Focus 25(5):E2
79. Safford KM, Safford SD, Gimble JM et al (2004) Characterization of neuronal/glial differentiation of murine adipose-derived adult stromal cells. Exp Neurol 187:319-328
80. Safwani WK, Makpol S, Sathapan S et al (2012) The impact of long-term in vitro expansion on the senescence-associated markers of human adipose-derived stem cells. Appl Biochem Biotechnol 166:2101-2113
81. Sakaguchi Y, Sekiya I, Yagishita K et al (2005) Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 52:2521-2529
82. Savitz SI, Dinsmore JH, Wechsler LR et al (2004) Cell therapy for stroke. NeuroRx 1:406-414
83. Schipper BM, Marra KG, Zhang W et al (2008) Regional anatomic and age effects on cell function of human adipose-derived stem cells. Ann Plast Surg 60:538-544
84. Sekhon LH, Fehlings MG (2001) Epidemiology, demographics, and pathophysiology of acute spinal cord injury spine (Phila Pa 1976) 26(24 Suppl):S2-12
85. Seo BM, Miura M, Gronthos S et al (2004) Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 364:149-155
86. Shi M, Ishikawa M, Kamei N et al (2009) Acceleration of skeletal muscle regeneration in a rat skeletal muscle injury model by local injection of human peripheral blood-derived CD133-positive cells. Stem Cells 27:949-960
87. Slaper-Cortenbach IC (2008) Current regulations for the production of multipotent mesenchymal stromal cells for clinical application. Transfus Med Hemother 35:295-298
88. Smith P, Adams WP Jr, Lipschitz AH et al (2006) Autologous human fat grafting: effect of harvesting and preparation techniques on adipocyte graft survival. Plast Reconstr Surg 117:1836-1844
89. Soncini M, Vertua E, Gibelli L et al (2007) Isolation and characterization of mesenchymal cells from human fetal membranes. J Tissue Eng Regen Med 1:296-305
90. Song L, Young NJ, Webb NE et al (2005) Origin and characterization of multipotential mesenchymal stem cells derived from adult human trabecular bone. Stem Cells Dev 14:712-721
91. Sterodimas A, de Faria J, Nicaretta B et al (2010) Tissue engineering with adipose-derived stem cells (ADSCs): current and future applications. J Plast Reconstr Aesthet Surg 63:1886-1892
92. Takamori Y, Mori T, Wakabayashi T et al (2009) Nestin-positive microglia in adult rat cerebral cortex. Brain Res 1270:10-18
93. Taléns-Visconti R, Bonora A, Jover R et al (2006) Hepatogenic differentiation of human mesenchymal stem cells from adipose tissue in comparison with bone marrow mesenchymal stem cells. World J Gastroenterol 12:5834-5845
94. Tator CH (1995) Update on the pathophysiology and pathology of acute spinal cord injury. Brain Pathol 5:407-413
95. Tholpady SS, Llull R, Ogle RC et al (2006) Adipose tissue: stem cells and beyond. Clin Plast Surg 33:55-62
96. Timper K, Seboek D, Eberhardt M et al (2006) Human adipose tissue-derived mesenchymal stem cells differentiate into insulin, somatostatin, and glucagon expressing cells. Biochem Biophys Res Commun 341:1135-1140
97. Todorov P, Hristova E, Konakchieva R et al (2010) Comparative studies of different cryopreservation methods for mesenchymal stem cells derived from human fetal liver. Cell Biol Int 34:455-462
98. Tohda C, Kuboyama T (2011) Current and future therapeutic strategies for functional repair of spinal cord injury. Pharmacol Ther 132:57-71
99. Toma JG, McKenzie IA, Bagli D et al (2005) Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 23:727-737
100. Traktuev DO, Merfeld-Clauss S, Li J et al (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. Circ Res 102:77-85
101. van Harmelen V, Skurk T, Röhrig K et al (2003) Effect of BMI and age on adipose tissue cellularity and differentiation capacity in women. Int J Obes Relat Metab Disord 27:889-895
102. Vindigni V, Michelotto L, Lancerotto L et al (2009) Isolation method for a stem cell population with neural potential from skin and adipose tissue. Neurol Res (Epub ahead of print)
103. Williams SK, McKenney S, Jarrell BE (1995) Collagenase lot selection and purification for adipose tissue digestion. Cell Transplant 4:281-289
104. Yen AH, Sharpe PT (2008) Stem cells and tooth tissue engineering. Cell Tissue Res 331:359-372
105. Yuan A, Rao MV, Sasaki T et al (2006) Alpha-internexin is structurally and functionally associated with the neurofilament triplet proteins in the mature CNS. J Neurosci 26:10006-10019
106. Zachar V, Rasmussen JG, Fink T (2011) Isolation and growth of adipose tissue-derived stem cells. Methods Mol Biol 698:37-49
107. Zannettino AC, Paton S, Arthur A et al (2008) Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 214:413-421
108. Zavan B, Vindigni V, Gardin C et al (2010a) Neural potential of adipose stem cells. Discov Med 10:37-43
109. Zavan B, Michelotto L, Lancerotto L et al (2010b) Neural potential of a stem cell population in the adipose and cutaneous tissues. Neurol Res 32:47-54
110. Zeidán-Chuliá F, Noda M (2009) "Opening" the mesenchymal stem cell tool box. Eur J Dent 3:240-249
111. Zuk PA, Zhu M, Mizuno H et al (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211-228
112. Zuk PA, Zhu M, Ashjian P et al (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279-4295