Cytogenetic studies of mesenchymal stem cells in rabbit: A mini-review

Main Article Content

J. Curlej
M. Tomková
J. Vasicek
P. Chrenek

Abstract

The aim of the present review is to summarize current knowledges of in vitro studies, focused on the determination of rabbit stem cells of different origin, based on their cytogenetic examination. Stem cells represent valuable model to study the biological traits or processes of health and targeted tissues, affected by various internal or external detrimental factors. Furthermore, these cells provide a promising mechanism of treatment of existing human or animal diseases. Although recent knowledges based on serious in vitro studies bring positive promises, there are still remained a lot of issues focused to the safety of stem cell usage in the context of their clinical application. In this way, the stability of the genome across individual generations of passaged cells plays an important role, evaluated on the basis of chromosomal profile, including aneuploidy and structural studies. In the given context, various culture conditions and manipulations among the studies play a crucial role in the definition of the final chromosomal status. Up to date, there are numbers of reliable animal models used as donors of embryonic or somatic stem cells. In this way, the rabbit represents an available source with numerous advantages for cytogenetic analysis.

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References

ASADI-YOUSEFABAD, S.L. – KHODAKARAMTAFTI, A. – DIANATPOUR, M. – MEHRABANI, D. – ZARE, S.H. – TAMADON, A. – NIKEGHBALIAN, S. – RAAYAT-JAHROMI, A. – AHMADLOU, S. 2015. Genetic evaluation of bone marrow-derived mesenchymal stem cells by a modified karyotyping method. Comparative Clinical Pathology, vol. 24 (6), 2015, p. 1361–1366.

BEN-DAVID, U. – BENVENISTY, N. 2012. High prevalence of evolutionarily conserved and species-specific genomic aberrations in mouse pluripotent stem cells. Stem Cells, vol. 30, 2012, p. 612–622.

BERNARDO, M.E. – ZAFFARONI, N. – NOVARA, F. – COMETA, A.M. – AVANZINI, M.A. – MORETTA, A. – MONTAGNA, D. – MACCARIO, R. – VILLA, R. – DAIDONE, M.G. – ZUFFARDI, O. – LOCATELLI, F. 2007. Human bone marrow derived mesenchymal stem cells do not undergo transformation after long-term in vitro culture and do not exhibit telomere maintenance mechanisms. Cancer Research, vol. 67, 2007, p. 9142–9149.

BORGONOVO, T. – MAY-VAZ, I. – SENEGAGLIA, A.C. – KUNIYOSHI-REBELATTO, C. L. – SLUDBROFMAN, P.R. 2014. Genetic evaluation of mesenchymal stem cells by G-banded karyotyping in a cell technology center. Revista Brasileira de Hematologia e Hemoterapia, vol. 36 (3), 2014, p. 202–207.

BUZZARD, J.J. – GOUGH, N.M. – CROOK, J.M. – COLMAN, A. 2004. Karyotype of human ES cells during extended culture. Nature Biotechnology, vol. 22, 2004, p. 381–382.

CATALINA, P. – COBO, F. – CORTÉS, J.L. – NIETO, A.I. – CABRERA, C. – MONTES, R. – CONCHA, A. – MENENDEZ, P. 2007. Conventional and molecular cytogeneticdiagnostic methods in stem cell research: a concise review. Cell Biology International, vol. 31, 2007, p. 861–869.

COCKBURN, K. – ROSSANT, J. 2010. Making the blastocyst: lessons from the mouse. The Journal of Clinical Investigation, vol. 120, 2010, p. 995–1003.

COWAN, C.A. – KLIMANSKAYA, I. – MCMAHON, J. – ATIENZA, J. – WITMYER, J. – ZUCKER, J.P. – WANG, S. – MORTON, C.C. – MCMAHON, A.P. – POWERS, D. – MELTON, D.A. 2004. Derivation of embryonic stem-cell lines from human blastocysts. The New England Journal of Medicine, vol. 350, 2004, p. 1353–1356.

DRAPER, J.S. – SMITH, K. – GOKHALE, P. – MOORE, H.D. – MALTBY, E. – JOHNSON, J. – MEISNER, L. – ZWAKA, T.P. – THOMSON, J.A. – ANDREWS, P.W. 2004. Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nature Biotechnology, vol. 22, 2004, p. 53–54.

ESTRADA, J.C. – ALBO, C. – BENGURÍA, A. – DOPAZO, A. – LÓPEZ-ROMERO, P. – CARRERA-QUINTANAR, L. – ROCHE, E. – CLEMENTE, E.P. – ENRÍQUEZ, J.A. – BERNAD, A. – SAMPER, E. 2012. Culture of human mesenchymal stem cells at low oxygen tension improves growth and genetic stability by activating glycolysis. Cell Death and Differentiation, vol. 19, 2012, p. 743–755.

FANG, Z.F. – GAI, H. – HUANG, Y.Z. – LI, S.G. – CHEN, X. J. – SHI, J.J. – WU, L. – LIU, A. – XU, P. – SHENG, H.Z. 2006. Rabbit embryonic stem cell lines derived from fertilized, parthenogenetic or somatic cell nuclear transfer embryos. Experimental Cell Research, vol. 312, 2006, p. 3669–3682.

FORSYTH, N.R. – MUSIO, A. – VEZZONI, P. – SIMPSON, A.H. – NOBLE, B.S. – MCWHIR, J. 2006. Physiologic oxygen enhances human embryonic stem cell clonal recovery and reduces chromosomal abnormalities. Cloning Stem Cells, vol. 8, 2006, p. 16–23.

FRANCO-LAMBERT, A.P. – FRAGA-ZANDONAI, A. – BONATTO, D. – CANTARELLI-MACHADO, D. – PÊGAS-HENRIQUES, J.A. 2009. Differentiation of human adipose-derived adult stem cells into neuronal tissue: does it work? Differentiation, vol. 77, 2009, p. 221–228.

GROMPE M. 2012. Tissue stem cells: new tools andfunctional diversity. Cell Stem Cell, vol. 10, 2012, p. 685–689.

GUO, J. – JAUCH, A. – HEIDI, H.G. – SCHOELL, B. – ERZ, D. – SCHRANK, M. – JANSSEN, J. W. 2005. Multicolor karyotype analyses of mouse embryonic stem cells. In Vitro Cellular & Developmental Biology. Animal, vol. 41, 2005, p. 278–283.

HOLZWARTH, C. – VAEGLER, M. – GIESEKE, F. – PFISTER, S.M. – HANDGRETINGER, R. – KERST, G. – MÜLLER, I. 2010. Low physiologic oxygen tensions reduce proliferation and differentiation of human multipotent mesenchymal stromal cells. BMC Cell Biology, vol. 11, 2010, pp. 11.

IMREH, M.P. – GERTOW, K. – CEDERVALL, J. – UNGER, C. – HOLMBERG, K. – SZÖKE, K. – CSÖREGH, L. – FRIED, G. – DILBER, S. – BLENNOW, E. – AHRLUND-RICHTER, L. 2006. In vitro culture conditions favouring selection of chromosomal abnormalities in human ES cells. Journal of Cellular Biochemistry, vol. 99, 2006, p. 508–516.

INZUNZA, J. – GERTOW, K. – STRÖMBERG, M.A. – MATILAINEN, E. – BLENNOW, E. – SKOTTMAN, H. – WOLBANK, S. – AHRLUND-RICHTER, L. – HOVATTA, O. 2005. Derivation of human embryonic stem cell lines in serum replacement medium using postnatal human fibroblasts as feeder cells. Stem Cells, vol. 23, 2005, p. 544–549.

JIANG, Y. – JAHAGIRDAR, B.N. – REINHARDT, R.L. – SCHWARTZ, R.E. – KEENE, C.D. – ORTIZ-GONZALEZ, X.R. – REYES, M. – LENVIK, T. – LUND, T. – BLACKSTAD, M. – DU, J. – ALDRICH, S. – LISBERG, A. – LOW, W. C. – LARGAESPADA, D.A. – VERFAILLIE, C.M. 2002. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature, vol. 418, 2002, p. 41–49.

JIN, H. – BAE, Y. – KIM, M. – KWON, S. – JEON, H. – CHOI, S. – KIM, S. – YANG, Y. – OH, W. – CHANG, J. 2013. Comparative analysis of human mesenchymal stem cells from bone marrow, adipose tissue, and umbilical cord blood as sources of cell therapy. International Journal of Molecular Sciences, vol. 14, p. 17986–18001.

KANG, B.J. – RYU, H.H. – PARK, S.S. – KOYAMA,Y. – KIKUCHI, M. – WOO, H.M. – KIM, W.H. – KWEON, O.K. 2012. Comparing the osteogenic potential of canine mesenchymal stem cells derived from adipose tissues, bone marrow, umbilical cord blood, and Wharton's jelly for treating bone defects. TL ─ 13. Journal of Veterinary Science, vol. 13 (3), 2012, p. 299–310.

KATARI, R. – PELOSO, A. – ORLANDO, G. 2015. Tissue engineering and regenerative medicine: semantic considerations for an evolving paradigm. Frontiers in Bioengineering and Biotechnology, vol. 2, 2015, pp. 57.

KOVAC, M. – VASICEK, J. – KULIKOVA, B. – BAUER, M. – CURLEJ, J. – BALAZI, A. – CHRENEK, P. 2017. Different RNA and protein expression of surface markers in rabbit amniotic fluid-derived mesenchymal stem cells. Biotechnology Progress, vol. 33 (6), 2017, p. 1601–1613.

LEFORT, N. – FEYEUX, M. – BAS, C. – FÉRAUD, O. – BENNACEUR-GRISCELLI, A. – TACHDJIAN, G. – PESCHANSKI, M. – PERRIER, A.L. 2008. Human embryonic stem cells reveal recurrent genomic instability at 20q11.21. Nature Biotechnology, vol. 26, 2008, p. 1364–1366.

LI, P. – TONG, C. – MEHRIAN-SHAI, R. – JIA, L. – WU, N. – YAN, Y. – MAXSON, R.E. – SCHULZE, E.N. – SONG, H. – HSIEH, C.L. – PERA, M.F. – YING, Q.L. 2008. Germline competent embryonic stem cells derived from rat blastocysts. Cell, vol. 135, 2008, p. 1299–1310.

LI, R. – CHEN, B. – WANG, G. – YU, B. – REN, G. – NI, G. 2011. Effects of mechanical strain on oxygen free radical system in bone marrow mesenchymal stem cells from children. Injury, vol. 42, 2011, p. 753–757.

LIM, H.J. – HAN, J. – WOO, D.H. – KIM, S.E. – KIM, S. K. – KANG, H.G. – KIM, J.H. 2011. Biochemical and morphological effects of hypoxic environment on human embryonic stem cells in long-term culture and differentiating embryoid bodies. Molecules and Cells, vol. 31, 2011, p. 123–132.

LUDWIG, T.E. – LEVENSTEIN, M.E. – JONES, J.M. – BERGGREN, W.T. – MITCHEN, E.R. – FRANE, J.L. – CRANDALL, L.J. – DAIGH, C.A. – CONARD, K.R. – PIEKARCZYK, M.S. – LLANAS, R.A. – THOMSON, J.A. 2006. Derivation of human embryonic stem cells in defined conditions. Nature Biotechnology, vol. 24, 2006, p. 185–187.

MAITRA, A. – ARKING, D.E. – SHIVAPURKAR, N. – IKEDA, M. – STASTNY, V. – KASSAUEI, K. – SUI, G. – CUTLER, D.J. – LIU, Y. – BRIMBLE, S.N. – NOAKSSON, K. – HYLLNER, J. – SCHULZ, T.C. – ZENG, X. – FREED, W.J. – CROOK, J. – ABRAHAM, S. – COLMAN, A. – SARTIPY, P. – MATSUI, S. – CARPENTER, M. – GAZDAR, A.F. – RAO, M. – CHAKRAVARTI, A. 2005. Genomic alterations in cultured human embryonic stem cells. Nature Genetics, vol. 37, 2005, p. 1099–1103.

MERKLE, F.T. – EGGAN, K. 2013. Modelling human disease with pluripotent stem cells: from genome association to function. Cell Stem Cell, vol. 12, 2013, p. 656–668.

MITALIPOVA, M.M. – RAO, R.R. – HOYER, D.M. – JOHNSON, J.A. – MEISNER, L.F. – JONES, K.L. – DALTON, S. – STICE, S.L. 2005. Preserving the genetic integrity of human embryonic stem cells. Nature Biotechnology, vol. 23, 2005, p. 19–20.

OLIVEIRA, P.H. – BOURA, J.S. – ABECASIS, M.M. – GIMBLE, J.M. – DA SILVA, C.L. – CABRAL, J.M. 2012. Impact of hypoxia and long-term cultivation on the genomic stability and mitochondrial performance of ex vivo expanded human stem/stromal cells. Stem Cell Research, vol. 9, 2012, p. 225–236.

OLIVEIRA, P.H. – DA SILVA, C.L. – CABRAL, J.M. 2014. Concise review: Genomic instability in human stem cells: current status and future challenges. Stem Cells, vol. 32, 2014, p. 2824–2832.

PITTENGER, M.F. – MARTIN, B. J. 2004. Mesenchymal stem cells and their potential as cardiac therapeutics. Circulation Research, vol. 95, 2004, p. 9–20.

PONTIKOGLOU, C. – DESCHASEAUX, F. – SENSEBÉ, L. – PAPADAKI, H.A. 2011. Bone marrow mesenchymal stem cells: biological properties and their role in hematopoiesis and hematopoietic stem cell transplantation. Stem Cell Reviews, 2011, vol. 7 (3), 2011, p. 569–589.

REBUZZINI, P. – NERI, T. – ZUCCOTTI, M. – REDI, C.A. – GARAGNA, S. 2008. Chromosome number variation in three mouse embryonic stem cell lines during culture. Cytotechnology, vol. 58, 2008, p. 17–23.

REBUZZINI, P. – ZUCCOTTI, M. – REDI, C.A. – GARAGNA, S. 2011. Genome stability in embryonic stem cells. Recent Advantages in Pluripotent Stem Cell-Based Regenerative Medicine, p. 399–410.

REBUZZINI, P. – ZUCCOTTI, M. – REDI, C.A. – GARAGNA, S. 2015. Chromosomal Abnormalities in Embryonic and Somatic Stem Cells. Cytogenetic and Genome Research, vol. 147 (1), 2015, p. 1–9.

SEILER, A.E. – SPIELMANN, H. 2011. The validated embryonic stem cell test to predict embryotoxicity in vitro. Nature Protocols, vol. 6, 2011, p. 961–978.

SENSEBÉ, L. – TARTE, K. – GALIPEAU, J. – KRAMPERA, M. – MARTIN, I. – PHINNEY, D.G. – SHI, Y. 2012. MSC Committee of the International Society for Cellular Therapy: Limited acquisition of chromosomal aberrations in human adult mesenchymal stromal cells. Cell Stem Cell, vol. 10, 2012, p. 9–10.

SOUKUP, T. – MOKRÝ, J. – KARBANOVÁ, J.– PYTLÍK, R. – SUCHOMEL, P. – KUCEROVÁ, L. 2006. Mesenchymal Slovak J. Anim. Sci., 51, 2018 (4): 150–155 Mini-review The 6th International Scientific Conference “Animal Biotechnology 2018” stem cells isolated from the human bone marrow: cultivation, phenotypic analysis and changes in proliferation kinetics. Acta Medica (Hradec Kralove), vol. 49, 2006, p. 27–33.

SUEMORI, H. – YASUCHIKA, K. – HASEGAWA. K. – FUJIOKA, T. – TSUNEYOSHI, N. – NAKATSUJI, N. 2006. Efficient establishment of human embryonic stem cell lines and long-term maintenance with stable karyotype by enzymatic bulk passage. Biochemical and Biophysical Research Communications, vol. 345, 2006, p. 926–932.

SUGAWARA, A. – GOTO, K. – SOTOMARU, Y. – SOFUNI, T. – ITO, T. 2006. Current status of chromosomal abnormalities in mouse embryonic stem cell lines used in Japan. Comparative Medicine, vol. 56, 2006, p. 31–34.

TILL, J.E. – MCCULLOUGH, E.A. 1961. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiation Research, vol. 14, 1961, p. 213–222.

TOMKOVA, M. – VASICEK, J. – KULIKOVA, B. – BALAZI, A. – CHRENEK, P. 2017. Comparison of rabbit endothelial progenitor cells and mesenchymal stem cells: cytogenetic approach. Slovak Journal of Animal Science, vol. 50 (2), 2017, p. 73–76.

TSAI, C.C. – CHEN, Y.J. – YEW, T.L. – CHEN, L.L. – WANG, J. Y. – CHIU, C.H. – HUNG, S.C. 2011. Hypoxia inhibits senescence and maintains mesenchymal stem cell properties through down-regulation of E2A-p21 by HIF-TWIST. Blood, vol. 117, 2011, p. 459–469.

UEYAMA, H. – HORIBE, T. – HINOTSU, S. – TANAKA, T. – INOUE, T. – URUSHIHARA, H. – KITAGAWA, A. – KAWAKAMI, K. 2012. Chromosomal variability of human mesenchymal stem cells cultured under hypoxic conditions. Journal of Cellular and Molecular Medicine, vol. 16, 2012, p. 72–82.

WANG, S. – TANG, X. – NIU, Y. – CHEN, H. – LI, B. – LI, T. – ZHANG, X. – HU, Z. – ZHOU, Q. – JI, W. 2007. Generation and characterization of rabbit embryonic stem cells. Stem Cells, vol. 25, 2007, p. 481–489.

ZHANG, Z.X. – GUAN, L.X. – ZHANG, K. – WANG, S. – CAO, P.C. – WANG, Y.H. – WANG, Z. – DAI, L.J. 2007. Cytogenetic analysis of human bone marrow-derived mesenchymal stem cells passaged in vitro. Cell Biology International, vol. 31, 2007, p. 645–648.

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