From blastomeres to somatic cells: reflections on cell developmental potential in light of chimaera studies - a review

• Autorzy: Zyzynska-Galenska K. , Piliszek A. , Modlinski J.A.
• Języki publikacji: EN

Abstrakty

EN

Mammalian development is a process, whereby cells from a totipotent zygote gradually lose their potency, i.e. their ability to differentiate, in the environment of the developing embryo. An ideal model for testing the real potential of cells is the experimental production of chimaeras. The first experimentally produced mammalian (murine) chimaeras were created by Tarkowski [1961] and since then many new methods of chimaera production have been developed, including injecting cells into the blastocyst’s cavity or into cleaving embryos. This review describes how different cell types, depending on the developmental stage or culture conditions, manifest their potential to contribute to chimaeras. Cell developmental potential has been analysed in pluripotent blastomeres, which can contribute to all embryonic and extra-embryonic lineages, albeit differently depending on their developmental stage. This is the case in blastocyst lineages, with various developmental potentials depending on the surrounding cells, and in more differentiated cells from different stages of pregnancy, which in some cases may colonise chimaeric animal tissue. Cell potential has also been analysed in embryonic stem and embryonal carcinoma cells, which are pluripotent and efficiently contribute to chimaeras; in multipotent fetal and adult stem cells, which can also participate in chimaera formation; and in somatic mouse embryonic fibroblasts (MEFs), which can also be reprogrammed in the environment of the cleaving embryo. Interspecies chimaera studies have also demonstrated the pluripotency of foreign cells. Experiments with chimaeras have shown that not only pluripotent embryonic cells are capable of contributing to chimaeras, so are adult cells, which plasticity is now well-documented.

Słowa kluczowe

EN

mammal; animal development; blastomere; somatic cell; cell development; development potential; chimaera; cell plasticity; pluripotency; stem cell

• Wydawca: -
• Czasopismo: Animal Science Papers and Reports
• Rocznik: 2017
• Tom: 35
• Numer: 3
• Opis fizyczny: p.225-240,fig.,ref.

Twórcy

autor

Zyzynska-Galenska K.

• Department of Experimental Embryology, Institute of Genetics and Animal Breeding, Polish Academy of Sciences, Jastrzebiec, 05-551 Magdalenka, Poland

autor

Piliszek A.

• Department of Experimental Embryology, Institute of Genetics and Animal Breeding, Polish Academy of Sciences, Jastrzebiec, 05-551 Magdalenka, Poland

autor

Modlinski J.A.

• Department of Experimental Embryology, Institute of Genetics and Animal Breeding, Polish Academy of Sciences, Jastrzebiec, 05-551 Magdalenka, Poland

Bibliografia

• 1. ANDEREGG C., MARKERT C. L., 1986 - Successful rescue of microsurgically produced homozygous uniparental mouse embryos via production of aggregation chimeras. Proceedings of the National Academy of Sciences of the United States of America 83(17), 6509 - 13.
• 2. BABINET C., 1980 A - simplified method for mouse blastocyst injection. Experimental Cell Research 130: 15 - 19.
• 3. BEDDINGTON R. S., ROBERTSON E. J., 1989 - An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. Development 105(4), 733 - 7.
• 4. BONNICKSEN A. L., 2009 - Chimaeras, hybrids and interspecies research. Georgetown University Press, Washington D. C.
• 5. BRADLEY A., EVANS M., KAUFMAN M. H., ROBERTSON E., 1984 - Formation of germ line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 309, 255 - 256.
• 6. BRINSTER R. L., 1974 - The effect of cells transferred into the mouse blastocyst on subsequent development. The Journal of Experimental Medicine 140, 1049 - 1056.
• 7. BUEMO C. P., GAMBINI A., MORO L. N., HIRIART M. I., FERNÁNDEZ-MARTÍN R., COLLAS P., SALAMONE D. F., 2016 - Embryo Aggregation in Pig Improves Cloning Efficiency and Embryo Quality. PLoS One. 11(2), e0146390.
• 8. BURNSIDE A. S., COLLAS P., 2002 - Induction of Oct-3/4 espression in somatic cells by gap junction - mediated cAMP signalling from blastomeres. European Journal of Cell Biology 81, 585 - 591.
• 9. BUTLER J. E., ANDERSON G. B., BONDURANT R. H., PASHEN R. L., PENEDO M. C., 1987 - Production of ovine chimeras by inner cell mass transplantation. Journal of Animal Science 65(1), 317 - 24.
• 10. CLARKE D. L., JOHANSSON C. B., WILBERTS J., VERESS B., NILSSON E., KARLSTRÖM H., LENDAHL U., FRISEN J., 2000 - Generalized potential of adult neural stem cells. Science 288: 1660 - 1663.
• 11. CZONKOWSKA M., GUSZKIEWICZ A., PAPIS K., KOSSAKOWSKI M., DZIAK J., STĘŻYCKA E., 1988 - Chimerism between the sheep and the goat. Medycyna Weterynaryjna 7, 414 - 416, in Polish, with English summary.
• 12. FEHILLY C. B., WILLADSEN S. M., TUCKER E. M., 1984 - Interspecific chimaerism between sheep and goat. Nature 307(5952), 634 - 6.
• 13. FEHILLY C. B., WILLADSEN S. M., 1986 - Embryo manipulation in farm animals. Oxford Reviews of Reproductive Biology 8, 379 - 413.
• 14. GARDNER R. L., 1968 - Mouse chimeras obtained by the injection of cells into the blastocyst. Nature 220(5167), 596 - 7.
• 15. GARDNER R. L., LYON M. F., EVANS E. P., BURTENSHAW M. D., 1985 - Clonal analysis of X- chromosome inactivation and the origin of the germ line in the mouse embryo. Journal of embryology and experimental morphology 88, 349 - 503.
• 16. GARDNER R. L., MUNRO A. J., 1974 - Successful construction of chimaeric rabbit. Nature 250(462), 146 - 7.
• 17. GARDNER R. L., ROSSANT J., 1979 - Investigation of the fate of 4-5 day post-coitum mouse inner cell mass cells by blastocyst injection. Journal of embryology and experimental morphology 52, 141 - 52.
• 18. GEIGER H., SICK S., BONIFER C., MÜLLER A. M., 1998 - Globin gene expression is reprogrammed in chimeras generated by injecting adult hematopoietic stem cells into mouse blastocysts. Cell 93(6), 1055 - 65.
• 19. GRABAREK J. B., ŻYŻYŃSKA K., SAIZ N., PILISZEK A., FRANKENBERG S., NICHOLS J., HADJANTONAKIS A. K., PLUSA B., 2012 - Differential plasticity of epiblast and primitive endoderm precursors within the ICM of the early mouse embryo. Development 139(1), 129 - 39.
• 20. HARDER F., HENSCHLER R., JUNGHAHN I., LAMERS M. G., MÜLLER A. M., 2002 - Human hematopoiesis in murine embryos after injecting human cord blood-derived hematopoietic stem cells into murine blastocysts. Blood 99, 719 - 721.
• 21. HARDER F., KIRCHHOF N., PETROVIC S., WIESE S., MÜLLER A. M., 2004 - Erythroid-like cells from neural stem cells injected into blastocysts. Experimental Hematology 32(7), 673 - 82.
• 22. JAMES R. M., KLERKX A. H., KEIGHREN M., FLOCKHART J. H., WEST J. D., 1995 - Restricted distribution of tetraploid cells in mouse tetraploid<==>diploid chimaeras. Developmental Biology 167, 213 - 226.
• 23. 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 14; 447(7146), 879 - 80.
• 24. KARASIEWICZ J., SACHARCZUKM., WAS B., GUSZKIEWICZ A., KORWIN-KOSSAKOWSKI M., GÓRNIEWSKA M., SZABLISTY E., MODLIŃSKI J. A., 2008 - Experimental embryonic-somatic chimaerism in the sheep confirmed by random amplified polymorphic DNA assay. The International Journal of Developmental Biology 52(2-3), 315 - 22.
• 25. KUES W. A., PETERSEN B., MYSEGADES W., CARNWATH J. W., NIEMANN H., 2005 - Isolation of murine and porcine fetal stem cells from somatic tissue. Biology of Reproduction 72(4), 1020 - 8.
• 26. LEE S. T., GONG S .P., YUM K. E., LEE E. J., LEE C. H., CHOI J .H., KIM D. Y., HAN H., KIM K. S., HYSOLLI E., AHN J. Y., PARK I. H., HAN J. Y., JEONG J. W., LIM J. M., 2013 - Transformation of somatic cells into stem cell-like cells under a stromal niche. The FASEB Journal 27(7), 2644 - 56.
• 27. MACKAY G. E., WEST J. D, 2005 - Fate of tetraploid cells in 4n<-->2n chimeric mouse blastocysts. Mechanisms of Development 122: 1266 - 1281.
• 28. MANN J. R., STEWART C. L., 1991 - Development to term of mouse androgenetic aggregation chimeras. Development 113(4), 1325 - 33.
• 29. MAYER J. F., FRITZ H. I., 1974 - The culture of preimplantation rat embryos and the production of allophonic rats. Journal of Reproduction and Fertility 39 (1), 1 - 9.
• 30. MCLAREN A., 1972 - Numerology of development. Nature 239, 274 - 276.
• 31. MEINECKE-TILLMAN S., MEINECKE B., 1984 - Experimental chimaeras - removal of reproductive barrier between sheep and goat. Nature 307(5952), 637 - 8.
• 32. MINTZ B., 1962 - Formation of genetically mosaic mouse embryos. American Zoologist 2, 432.
• 33. MINTZ B., 1965 - Genetic mosaicism in adult mice of quadriparental lineage. Science 148 (3674), 1232 - 3.
• 34. MINTZ B., ILLMENSEE K., 1975 - Normal genetically mosaic mice produced from malignant teratocarcinoma cells. Proceedings of the National Academy of Sciences of the United States of America 72, 3585 - 3589.
• 35. MOUSTAFA L. A., BRINSTER R. L., 1972 - Induced chimaerism by transplanting embryonic cells into mouse blastocysts. J. Exp. Zool. 181, 193 - 202.
• 36. MOUSTAFA L. A., BRINSTER R. L. -1972 - The fate of transplanted cells in mouse blastocysts in vitro. Journal of Experimental Zoology 181, 181 - 192.
• 37. MYSTKOWSKA E. T., 1975 - Development of mouse-bank vole interspecific chimaeric embryos. Journal of embryology and experimental morphology 33(3), 731 - 44.
• 38. NAGY A., GOCZA E., DIAZ E. M., PRIDEAUX V. R., IVANYI E., MARKKULA M., ROSSANT J., 1990 - Embryonic stem cells alone are able to support fetal development in the mouse. Development 110, 815 - 821.
• 39. PAPAIOANNOU V. E., MCBURNEY M. W., GARDNER R. L., EVANS M. J., 1975 - Fate of teratocarcinoma cells injected into early mouse embryos. Nature 258, 70 - 72.
• 40. PESSAC B., NIMMAGADDA V. K., MAKAR T., FISHMAN P. S., BEVER C. T. JR, TRISLER D., 2012 - Adult hematopoietic progenitors are multipotent in chimeric mice. Comptes Rendus Biologies 335(7), 454 - 62.
• 41. PILISZEK A., MODLIŃSKI J. A., PYŚNIAK K., KARASIEWICZ J., 2007 - Foetal fibroblasts introduced to cleaving mouse embryos contribute to full-term development Reproduction 133 207 - 218.
• 42. PIOTROWSKA-NITSCHE K., PEREA-GOMEZ A., HARAGUCHI S., ZERNICKA-GOETZ M., 2005 - Four-cell stage mouse blastomeres have different developmental properties. Development 132(3), 479 - 90.
• 43. PIOTROWSKA-NITSCHE K., ZERNICKA-GOETZ M., 2004 - Spatial arrangement of individual 4-cell stage blastomeres and the order in which they are generated correlate with blastocyst pattern in the mouse embryo. Mechanisms of Development 122(4), 487 - 500.
• 44. PLUSA B., HADJANTONAKIS A. K., GRAY D., PIOTROWSKA-NITSCHE K., JEDRUSIK A., PAPAIOANNOU V. E., GLOVER D. M., ZERNICKA-GOETZ M., 2005 - The first cleavage of the mouse zygote predicts the blastocyst axis. Nature 434(7031), 391 - 5.
• 45. PRATHER R. S., FIRST N. L., 1987 - Developmental fate in chimeras derived from highly asynchronous murine blastomeres. Journal of Experimental Zoology 242(1), 27 33.
• 46. ROSSANT J., VIJH K. M., 1980 - Ability of outside cells from preimplantation mouse embryos to form inner cell mass derivatives. Development Biology 76, 475 - 482.
• 47. ROSSANT J., FRELS W. I., 1980 - Interspecific chimeras in mammals: successful production of live chimeras between Mus musculus and Mus caroli. Science 208(4442), 419 - 21.
• 48. SABURI S., AZUMA S., SATO E., TOYODA Y., TACHI C., 1997 - Developmental fate of single embryonic stem cells microinjected into 8-cell-stage mouse embryos Differentiation 62(1), 1 - 11.
• 49. SKRZYSZOWSKA M., SMORAG Z., SŁOMSKI R., KATSKA-KSIAZKIEWICZ L., KALAK R., MICHALAK E., WIELGUS K., LEHMANN J., LIPIŃSKI D., SZALATA M., PŁAWSKI A., SAMIEC M., JURA J., GAJDA B., RYŃSKA B., PIEŃKOWSKI M., 2006 - Generation of transgenic rabbits by the novel technique of chimeric somatic cell cloning. Biology of Reproduction 74(6), 1114 - 20.
• 50. SPINDLE A., 1982 - Cell allocation in preimplantation mouse chimeras. Journal of Experimental Zoology 219(3), 361 - 7.
• 51. STEVENS L. C., VARNUM D. S., EICHER E. M., 1977 - Viable chimaeras produced from normal and parthenogenetic mouse embryos. Nature 269(5628) : 515 - 7.
• 52. STEVENS L. C., 1978 - Totipotent cells of parthenogenetic origin in a chimaeric mouse. Nature 276(5685), 266 - 7.
• 53. STEWART C. L., 1982 - Formation of viable chimaeras by aggregation between teratocarcinomas and preimplantation mouse embryos. Journal of Embryology and Experimental Morphology 67, 167 - 179.
• 54. STEWART C. L., GADI I., BHATT H., 1994 - Stem cells from primordial germ cells can reenter the germ line. Developmental Biology 161, 626 - 628.
• 55. SUMMERS P. M., SHELTON J. N., BELL K., 1983 - Synthesis of primary Bos taurus - Bos indicus chimaeric calves. Animal Reproduction Science 6, 91 - 102.
• 56. SURANI M. A., BARTON S. C., HOWLETT S. K., NORRIS M. L., 1988 - Influence of chromosomal determinants on development of androgenetic and parthenogenetic cells. Development 103(1), 171 - 8.
• 57. SURANI M. A., BARTON S. C., KAUFMAN M. H., 1977 - Development to term of chimaeras between diploid parthenogenetic and fertilised embryos. Nature 270(5638), 601 - 3.
• 58. SUWIŃSKA A., CZOŁOWSKA R., OZDZEŃSKI W., TARKOWSKI A. K., 2008 - Blastomeres of the mouse embryo lose totipotency after the fifth cleavage division: expression of Cdx2 and Oct4 and developmental potential of inner and outer blastomeres of 16 - and 32 - cell embryos. Developmental Biology 322(l) : 133 - 44. Erratum in: Dev Biol. 2009 Jan 1; 325(1), 308.
• 59. SUWIŃSKA A., OZDZENSKI W., WAKSMUNDZKAK., TARKOWSKI A. K.„ 2005 - Exprimentally produced diploid-triploid chimaeras develop up to adulthood. Molecular Reproduction and Development 72(3), 362 - 376.
• 60. TAKAHASHI K.,YAMANAKA S., 2006 -. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663 - 676.
• 61. TARKOWSKI A. K., 1961 - Mouse chimaeras developed from fused eggs. Nature 190, 857 - 860.
• 62. TARKOWSKI A. K., SUWIŃSKA A., CZOŁOWSKA R., OŻDŻEŃSKI W, 2010 - Individual blastomeres of 16 - and 32 - cell Mouse embryos are able to develop into foetuses and mice. Developmental Biology 348(2), 190 - 8.
• 63. TARKOWSKI A. K., WITKOWSKA A., OPAS J., 1977 - Development of cytochalasin B-induced tetraploid and diploid/tetraploid mosaic mouse embryos. Journal of embryology and experimental morphology 41, 47 - 64.
• 64. THOMSON J. A., SOLTER D., 1988 - The developmental fate of androgenetic, parthenogenetic, and gynogenetic cells in chimeric gastrulating mouse embryos. Genes & Development 2(10), 1344 - 51.
• 65. TOKUNAGA T., TSUNODA Y., 1992 - Efficacious Production of Viable Germ-Line Chimeras between Embryonic Stem (ES) Cells and 8-Cell Stage Embryos Development, growth & differentiation 34 (5), 561 - 566.
• 66. WADDINGTON C. H., 1957 - The Strategy of the Genes. London: George Allen and Unwin.
• 67. WERNIG M., MEISSNER A., FOREMAN R., BRAMBRINK T., KU M., HOCHEDLINGER K., BERNSTEIN B. E. AND JAENISCH R., 2007 - In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448, 318 - 324.
• 68. WILLADSEN S. M., FEHILLY C. B., 1983 - The developmental potential and regulatory capacity of blastomeres from two-, four-and eight-cell sheep embryos. Fertilization of the Human Egg In Vitro 353 - 357.
• 69. WILLIAMS T. J., MUNRO R. K., SHELTON J. N., 1990 - Production of interspecies chimeric calves by aggregation of Bos indicus and Bos taurus demi-embryos. Reproduction, Fertility and Development 2, 385 - 394.
• 70. WU J., PLATERO-LUENGO A., SAKURAI M., SUGAWARA A., GIL M. A., YAMAUCHI T., SUZUKI K., BOGLIOTTI Y. S., CUELLO C., MORALES VALENCIA M., OKUMURA D., LUO J., VILARIŃO M., PARRILLA I., SOTO D. A., MARTINEZ C. A., HISHIDA T., SÁNCHEZ- BAUTISTA S., MARTINEZ-MARTINEZ M. L., WANG H., NOHALEZ A., ATZAWA E., MARTINEZ-REDONDO P., OCAMPO A., REDDY P., ROCA J., MAGA E. A., ESTEBAN C. R., BERGGREN W. T., NUNEZ DELICADO E., LAJARA J., GUILLEN I., GUILLEN P., CAMPISTOL J. M., MARTINEZ E. A., ROSS P. J., IZPISUA BELMONTE J. C., 2017 - Interspecies Chimerism with Mammalian Pluripotent Stem Cells. Cell 168(3), 473 - 486. el5.
• 71. XIANG A. P., MAO F. F., LI W. Q., PARK D., MA B. F., WANG T., VALLENDER T. W., VALLENDER E. J., ZHANG L., LEE J., WATERS J. A., ZHANG X. M., YU X. B., LI S. N., LAHN B. T., 2008 - Extensive contribution of embryonic stem cells to the development of an evolutionarily divergent host. Human Molecular Genetics 17(1), 27 - 37.
• 72. YANG X., ANDERSON G. B., 1992 - Micromanipulation of mammalian embryos: Principles, progress and future possibilities. Theriogenology 38(2), 315 - 35.
• 73. ZHAO M. T., BENNETT M. W., ZHANG X., SPATE L., WHITWORTH K. M., MURPHY C. N., RIEKE A., ZHANG Y., PRATHER R. S., 2010 - Contribution to neural and mesodermal lineages by porcine skin-derived progenitors (SKPs) in vivo. Cell Cycle 9(10), 2040 - 1.
• 74. ZHAO M. T., YANG X., LEE K., MAO J., TESON J. M., WHITWORTH K. M., SAMUEL M. S., SPATE L. D., MURPHY C. N., PRATHER R. S., 2012 - The In Vivo Developmental Potential of Porcine Skin-Derived Progenitors and Neural Stem Cells. Stem Cells and Development 21(14), 2682 - 8.
• 75. ŻYŻYŃSKA K., GRABAREK J., KARASIEWICZ J., MODLIŃSKI J. A., PLUSA B., 2013 - Reprogramming of somatic cells in embryonic environment. Reproductive Biology 13 (2), 62, (P6. 20).