Controversies about the chromosomal stability of cultivated mesenchymal stem cells: Their clinical use is it safe?

Current Stem Cell Research and Therapy

Volumn 7, Issue 5, 2012, Pages 356-363

  Ferreira, Reginaldo Justino ^a,b   Irioda, Ana Carolina ^c   Cunha, Ricardo Correa ^c   Francisco, Julio Cesar ^a,c   Guarita Souza, Luiz Cesar ^a   Srikanth, Garikipati Venkata Naga ^d   Nityanand, Soniya ^d   Rosati, Roberto ^c   Chachques, Juan Carlos ^e   de Carvalho, Katherine Athayde Teixeira ^a,c  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^b UNIVERSIDADE TECNOLÓGICA FEDERAL DO PARANÁ   (Brazil)

^c INSTITUTO DE PESQUISA PELÉ PEQUENO PRÍNCIPE   (Brazil)

^d SANJAY GANDHI POSTGRADUATE INSTITUTE OF MEDICAL SCIENCES   (India)

^e HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

Author keywords

Adult stem cell; Chromosomal abnormalities; FISH; Genetic screening; In vitro transformation; Karyotyping; MSC cultivation; Neoplastic transformation of MSC

Indexed keywords

FIBROBLAST GROWTH FACTOR;

ADULT STEM CELL; ANEUPLOIDY; CELL CULTURE; CELL DIFFERENTIATION; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATION; CHROMOSOME Q BAND; CHROMOSOME STRUCTURE; COMPARATIVE GENOMIC HYBRIDIZATION; DNA REPAIR; DNA SEQUENCE; FLOW CYTOMETRY; FLUORESCENCE IN SITU HYBRIDIZATION; HEMATOPOIETIC STEM CELL; HUMAN; KARYOTYPING; MESENCHYMAL STEM CELL; PAPANICOLAOU TEST; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ADULT STEM CELLS; ANIMALS; CELL CULTURE TECHNIQUES; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATIONS; GENETIC TESTING; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; REGENERATIVE MEDICINE;

EID: 84867033275     PISSN: 1574888X     EISSN: None     Source Type: Journal    
DOI: 10.2174/157488812802481472     Document Type: Review

References (72)

1. Bernardo ME, Zaffaroni N, Novara F, et al. Human bone marrowderived mesenchymal stem cells do not undergo transformation after long-term in vitro culture and do not exhibit telomere maintenance mechanisms. Cancer Res 2007; 67(19): 9142-9.
2. National Institute of Mental Health; University of Virginia. In: ClinicalTrials.gov [Internet]. Bethesda (MD): National Library of Medicine (USA) http://www.clinicaltrials.gov/ct2/search [Accessed October 10, 2011].
3. Somoza RA, Rubio FJ. Cell therapy using induced pluripotent stem cells or somatic stem cells: this is the question. Curr Stem Cell Res Ther 2012; 7(3): 191-196.
4. Umar S, de Visser YP, Steendijk P, et al. Allogenic stem cell therapy improves right ventricular function by improving lung pathology in rats with pulmonary hypertension. Am J Physiol Heart CircPhysiol 2009; 297: H1606-16.
5. Guarita-Souza LC, Francisco JC, Simeoni R, Faria-Neto JR, Carvalho KAT. Benefit of stem cells and skeletal myoblast cells in dilated cardiomyopathies. World J Cardiol 2011; 3(3): 93-7.
6. Williams AR, Hare JM. Msenchymal stem cells: biology, pathophysiology, translation findings and therapeutic implications for cardiac disease. Circ Res 2011; 109(8): 923-40.
7. Rodriguez A-M, Elabd C, Amriez Z, Ailhaud G, Dani C. The human adipose tissue is a source of multipotent stem cells. Biochimie 2005; 87(1): 125-8.
8. Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8(4):315-7.
9. Zhang Z-X, Guan L-X, Zhang K, et al. Cytogenetic analysis of human bone marrow-derived mesenchymal stem cells passaged in vitro. Cell BiolInt 2007; 31(6): 645-8.
10. Bochkov NP, Voronina ES, Kosyakova NV et al. Chromosome variability of human multipotent mesenchymal stromal cells. Bull Exp Biol Med 2007; 143(1): 122-6.
11. Bochkov NP, Nikitina VA, Buyanovskaya OA, et al. Aneuploidy of stem cells isolated from human adipose tissue. Bull Exp Biol Med 2008; 146(3): 344-7.
12. Meza-Zepeda LA, Noer A, Dahl JA, Micci F, Myklebost O, Collas P. High-resolution analysis of genetic stability of human adipose stem cells cultured to senescence. J Cell Mol Med 2008; 12(2): 553-63.
13. Buyanovskaya OA, Kuleshov NP, Nikitina VA, Voronina ES, Katosova LD, Bochkov NP. Spontaneous aneuploidy and clone formation in adipose tissue stem cells during different periods of culturing. Bull Exp Biol Med 2009; 148(1): 109-12.
14. Grimes BR, Steiner CM, Merfeld-Clauss S, et al. Interphase FISH demonstrates that human adipose stromal cells maintain a high level of genomic stability in long-term culture. Stem Cells Dev 2009; 18(5): 717-24.
15. Strauer BE, Kornowski R. Stem cell therapy in perspective. Circulation 2003; 107: 929-34.
16. Cottler-Fox MH, Lapidot T, Petit I, et al. Stem cell mobilization. Hematology 2003; 2003: 419-37.
17. Lee MS, Lill M, Makkar RR. Stem cell transplantation in myocardial infarction. Rev Cardiovasc Med 2004; 5(2): 729-37.
18. Horwitz EM, Le Blanc K, Dominici M, et al. Clarification of the nomenclature for MSC: the International Society for Cellular Therapy position statement. Cytotherapy 2005; 7(5): 393-5.
19. Moore TB, Campbell KJ, Feig SA. Stem cells carrying abnormal karyotype engraft after cord blood stem cell transplant. J Pediatr-HematolOncol 2005; 27(2): 118-9.
20. Strem BM, Hicok KC, Zhu M, et al. Multipotential differentiation of adipose tissue-derived stem cells. Keio J Med 2005; 54(3): 132-41.
21. Foroni C, Galli R, Cipelleti B, et al. Resilience to transformation and functional stability of adult neural stem cell ex vivo. Cancer Res 2007; 67: 3725-33.
22. Rubio D, Garcia-Castro J, Martín MC, et al. Spontaneous human adult stem cell transformation. Cancer Res 2005; 65: 3035-9.
23. Burns JS, Abdallah BM, Guldberg P, Rygaard J, Schroder HD, Kassem M. Tumorigenic heterogeneity in cancer stem cells evolved fromlong-term cultures of telomerase-immortalized human. Cancer Res 2005; 65: 3126-35.
24. Wagner W, Ho AD, Zenke M. Different facets of aging in humanmesenchymal stem cells. Tissue Eng Part B Rev 2010; 16: 445-53.
25. Achille V, Mantelli M, Arrigo G, et al. Cell-cycle phases and genetic profile of bone marrow-derive mesenchymal stromal cells expanded in vitro from healthy donors. J Cell Biochem 2011; 112(7): 1817-21.
26. Sensebé L, Tarte K, Krampera M, et al. Limited acquisition of chromosomal aberrations in human adult mesenchymal stromal cells. Cells Stem Cell 2012; 10(1): 9-10.
27. Ben-David U, Mayshar Y, Benvenisty N. Significant acquisition of chromosomal aberrations in human adult mesenchymal stromal cells: response to Sensebé et al. Cells Stem Cell 2012; 10(1): 10-11.
28. Buzzard JJ, Gough NM, Crook JM, Colman A. Karyotype of human ES cells during extended culture. Nat Biotechnol 2004; 22: 381-2.
29. Dahl J-A, Duggal S, Coulston N, et al. Genetic and epigenetic instability of human bone marrow mesenchymal stem cells expanded in autologous serum or fetal bovine serum. Int j Dev Biol 2008; 52: 1033-42.
30. Maitra A, Arking DE, Shivapurkar N, et al. Genomic alterations in cultured human embryonic stem cells. Nat Genet 2005; 37: 1099-103.
31. - mesenchymal stem cells: feasibility and safety from monkey to human. Stem Cells Dev 2006; 15(3): 349-57.
32. Izadpanah R, Kaushal D, Kriedt C, et al. Long-term in vitro expansion alters the biology of adult mesenchymal stem cells. Cancer Res 2008; 68: 4229-38.
33. Ra JC, Shin IS, Kim SH, et al. Safety of intravenous infusion of human adipose tissue-derived mesenchymal stem cells in animals and humans. Stem Cells Dev 2011; 20(8): 1297-308.
34. Tarte K, Gaillard J, Lataillade J-J, et al. Clinical-grade production of human mesenchymal stromal cells:occurrence of aneuploidy without transformation. Blood 2010; 115(8): 1549-53.
35. Bochkov NP, Nikitina VA, Voronina ES, Kuleshov NP. Methodological guidelines for genetic safety testing of cell transplants. Cell Tec Bio Med 2009; 148(4): 677-83.
36. Torsvik A, Røsland GV, Svendsen A, et al. Spontaneous malignant transformation of human mesenchymal stem cells reflects crosscontamination: putting the research field on track - letter. Cancer Res 2010; 70: 6393-6.
37. Fang X, Zhang P. Aneuploidy and tumorigenesis. Semin Cell Dev Biol 2011; 22(6): 595-601.
38. Crespo-Diaz R, Behfar A, Butler W, et al. Platelet lysate consisting of a natural repair proteosome supports human mesenchymal stem cell proliferation and chromosomal stability. Cell Transp 2011; 20: 797-811.
39. + cells. J Cell Mol Med 2011; 15(9): 1983-8.
40. Choumerianou DM, Dimitriou H, Perdikogianni C, Martimianaki G, Riminucci M, Kalmanti M. Study of oncogenic transformation in ex vivo expanded mesenchymal cells, from paediatric bone marrow. Cell Prolif 2008; 41(6): 909-22.
41. de la Fuente R, Bernad A, Garcia-Castro J, Martin MC, Cigudosa JC. Retraction: Spontaneous human adult stem cell transformation. Cancer Res 2010; 70(16): 6682.
42. Garcia S, Martín SC, de la Fuente R, Cigudosa JC, Garcia-Castro J, Bernad A. Pitfalls in spontaneous in vitro transformation of human mesenchymal stem cells. Exp Cell Res 2010; 316(9): 1648-50.
43. Izadpanah R, Trygg C, Patel B, et al. Biological properties of mesenchymal stem cells derived from bone marrow and adipose tissue. J Cell Biochem 2006; 99(5): 1285-97.
44. Guillot PV, Goterstrom C, Chan J, Kurata H, Fisk NM. Human first-trimester fetal MSC express pluripotency markers and grow faster and have longer telomeres than adult MSC. Stem Cells 2007, 25(3): 646-54.
45. Sethe S, Scutt A, Stolzing A. Aging of mesenchymal stem cells. Ageing Res Rev 2006; 5(1): 91-116.
46. Basel MF. ISCN: An Internacional System for Human Cytogenetics Nomenclature. Karger Publishers: Menphis 1995.
47. Léonard A, Rueff J, Gerber GB, Léonard ED. Usefulness and limits of biological dosimetry based on cytogenetic methods. Radiat Prot Dosimetry 2005; 115(1-4): 448-54.
48. Sra KK, Babb-Tarbox M, Aboutalebi S, et al. Molecular diagnosis of cutaneous diseases. Arch Dermatol 2005; 141(2): 225-41.
49. van der Berg C, van Opstal D, Polak-Knook J, Galjaard RJ. (Potential) false-negative diagnosis in chorionic villi and a review of the literature. Prenat Diagn 2006; 26(5): 401-8.
50. Pinkel D, Straume T, Gray J. Cytogenetic analyses using quantitative, high sensitive, fluorescence hybridization. Proc Natl Acad Sci 1986; 83(9): 2934-8.
51. Gersen SL, Keagle MB. The principles of clinical genetics. Human Press Inc: New Jersey 1999.
52. Schoumans J, Anderlid B-M, Blennow E, Teh BT, Nordenskjöld M. The performance of CGH array for the detection of cryptic constitutional chromosome imbalances. J Med Genet 2004; 41(3): 198-202.
53. Nowak NJ, Miecznikowski J, Moore SR, et al. Challenges in array comparative genomic hybridization for the analysis of cancer samples. Genet Med 2007; 9(9): 585-95.
54. Fan YS, Siu VM, Jung JH, Xu J. Sensitivity of multiple color spectral karyotyping in detecting small interchromosomal rearrangements. Genet Test 2000; 4(1): 9-14.
55. Heng HHQ, Ye CJ, Yang F, et al. Analysis of marker or complex chromosomal rearrangements present in pre-and post-natal karyotypes utilizing a combination of G-banding, spectral karyotyping and fluorescence in situ hybridization. Clin Genet 2003; 63(5): 358-67.
56. Ikeuchi T. Extending the capabilities of human chromosome analysis: from high-resolution banding to chromatin fiber-FISH. Hum Cell 1997; 10(2): 121-34.
57. Strachan T, Read AP. Human molecular genetics. 3rdEd. Garland Science: London 2003.
58. Lichtenbelt KD, Knoers NVAM, Schuring-Blom GH. From karyotyping to array-CGH in prenatal diagnosis. Cytogenet Genome Res 2011; 135(3-4): 241-50.
59. Røsland GV, Svendesen A, Torsvik A, et al. Long-term cultures of bone marrow-derived human mesenchymal stem cells frequently undergo spontaneous malignant transformation. Cancer Res 2009; 69: 5331-9.
60. Jeong JO, Han JW, Kim JM, et al. Malignant tumor formation after transplantation of short-term cultured bone marrow mesenchymal stem cells in experimental myocardial infarction and diabetic neuropathy. Circ Res 2011; 108(11): 1340-7.
61. Irioda AC, Zocche L, Souza CMCO, et al. Pap test as the first step in sreening genetic stability in cell-based therapy. J Stem Cell Res Ther 2011; 1: 3.
62. Estrada JC, Albo C, Benguría A, et al. Culture of human mesenchymal stem cells at low oxygen tension improves growth and genetic stability by activating glycolysis. Cell Death Differ 2011.
63. Ueyama H, Horibe T, Hinotsu S, et al. Chromosomal variability of human mesenchymal stem cells cultured under hypoxic conditions. J Cell Mol Med 2012; 16(1): 72-82.
64. Gotoh N. Control of stemness by fibroblast growth factor signaling in stem cells and cancer stem cells. Curr Stem Cell Res Ther 2009; 4(1): 9-15.
65. Maas SA, Donghia NM, Tompkins K, Foreman O, Mills KD. ARTEMIS stabilizes the genome and modulates proliferative responses in multipotent mesenchymal cells. BMC Biol 2010; 8: 132.
66. Quail DF, Taylor MJ, Postovit L-M. Microenvironmental regulation of cancer stem cell phenotypes. Curr Stem Cell Res Ther 2012; 7(3): 197-216.
67. Thirabanjasak D, Tantiwongse K, Thorener PS. Angiomyeloproliferative lesions following autologous stem cell therapy. J Am Soc Nephrol 2010; 21(7): 1218-22.
68. Imreh MP, Gertow K, Cedervall J, et al. In vitro culture conditions favoring selection of chromosomal abnormalities in human ES cells. J Cell Biochem 2006; 99(2): 508-16.
69. Catalina P, Montes R, Ligero G, et al. Human ESCs predisposition to karyotypic instability: Is a matter of culture adaptation or differential vulnerability among hESC lines due to inherent properties? Mol Cancer 2008; 7: 76.
70. Mohrin M, Bourke E, Alexander D, et al. Hematopoietic stem cell quiescence promotes error-prone DNA repair and mutagenesis. Cell Stem Cell 2010; 7(2): 174-85.
71. Chen Z, Zhao T, Xu Y. The genomic stability of induced pluripotent stem cells. Protein Cell 2012; 3(4): 271-7.
72. Harrison NJ. Genetic instability in neural stem cells: an inconvenient truth? J Clin Invest 2012; 122(2): 484-6.