Stem cells and interspecies chimaeras

Nature

Volumn 540, Issue 7631, 2016, Pages 51-59

  Wu, Jun ^a,b   Greely, Henry T ^c   Jaenisch, Rudolf ^d   Nakauchi, Hiromitsu ^e,f   Rossant, Janet ^g,h   Belmonte, Juan Carlos Izpisua ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b CATHOLIC UNIVERSITY OF MURCIA   (Spain)

^c STANFORD LAW SCHOOL   (United States)

^d WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF TOKYO   (Japan)

^g HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^h UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGY; CELLS AND CELL COMPONENTS; RESEARCH METHOD; SHARK;

BLASTOCYST; CELL SURVIVAL; CHIMERA; DEVELOPMENTAL BIOLOGY; DISEASE MODEL; DONOR; DRUG SCREENING; ETHICS; EVOLUTION; GENETIC COMPLEMENTATION; HUMAN; IN VIVO STUDY; LAW; NONHUMAN; ORGAN; PRIORITY JOURNAL; REVIEW; SPECIES COMPARISON; STEM CELL; ANIMAL; CELL LINEAGE; CYTOLOGY; EMBRYOLOGY; LEGISLATION AND JURISPRUDENCE; PRECLINICAL STUDY; SPECIES DIFFERENCE; STEM CELL RESEARCH;

CHIMAERIFORMES; MAMMALIA;

ANIMALS; BIOLOGICAL EVOLUTION; BLASTOCYST; CELL LINEAGE; CHIMERA; DRUG EVALUATION, PRECLINICAL; HUMANS; SPECIES SPECIFICITY; STEM CELL RESEARCH; STEM CELLS;

EID: 85000869911     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature20573     Document Type: Review

References (106)

1. Ito, R., Takahashi, T., Katano, I. & Ito, M. Current advances in humanized mousemodels. Cell. Mol. Immunol. 9, 208-214 (2012).
2. Le Douarin, N. M. The ontogeny of the neural crest in avian embryo chimaeras.Nature 286, 663-669 (1980).
3. Douarin, N. L. & Kalcheim, C. The Neural Crest (Cambridge Univ. Press, 1982).
4. Gardner, R. L. & Johnson, M. H. Investigation of early mammalian developmentusing interspecific chimaeras between rat and mouse. Nature 246, 86-89 (1973).
5. Rossant, J. & Frels, W. I. Interspecific chimeras in mammals: successfulproduction of live chimeras between Mus musculus and Mus caroli. Science208, 419-421 (1980).
6. Rossant, J., Vijh, M., Siracusa, L. D. & Chapman, V. M. Identification ofembryonic cell lineages in histological sections of M. musculus in-equilibriumM. caroli chimaeras. J. Embryol. Exp. Morphol. 73, 179-191 (1983).
7. Fehilly, C. B., Willadsen, S. M. & Tucker, E. M. Interspecific chimaerism betweensheep and goat. Nature 307, 634-636 (1984).
8. Williams, T. J., Munro, R. K. & Shelton, J. N. Production of interspecies chimericcalves by aggregation of Bos indicus and Bos taurus demi-embryos. Reprod.Fertil. Dev. 2, 385-394 (1990).
9. Rossant, J., Croy, B. A., Chapman, V. M., Siracusa, L. & Clark, D. A. Interspecificchimeras in mammals: a new experimental system. J. Anim. Sci. 55,1241-1248 (1982).
10. Rossant, J., Mauro, V. M. & Croy, B. A. Importance of trophoblast genotype forsurvival of interspecific murine chimeras. J. Embryol. Exp. Morphol. 69,141-149 (1982).
11. Wu, J. & Izpisua Belmonte, J. C. Dynamic pluripotent stem cell states and theirapplications. Cell Stem Cell 17, 509-525 (2015).
12. Xiang, A. P. et al. Extensive contribution of embryonic stem cells to thedevelopment of an evolutionarily divergent host. Hum. Mol. Genet. 17, 27-37(2008).
13. Han, X. et al. Forebrain engraftment by human glial progenitor cells enhancessynaptic plasticity and learning in adult mice. Cell Stem Cell 12, 342-353(2013).
14. Ying, Q.-L. et al. The ground state of embryonic stem cell self-renewal. Nature453, 519-523 (2008).
15. Buehr, M. et al. Capture of authentic embryonic stem cells from ratblastocysts. Cell 135, 1287-1298 (2008).
16. Li, P. et al. Germline competent embryonic stem cells derived from ratblastocysts. Cell 135, 1299-1310 (2008).
17. Kobayashi, T. et al. Generation of rat pancreas in mouse by interspecificblastocyst injection of pluripotent stem cells. Cell 142, 787-799 (2010).
18. Isotani, A., Hatayama, H., Kaseda, K., Ikawa, M. & Okabe, M. Formation of athymus from rat ES cells in xenogeneic nude mouse? rat ES chimeras. GenesCells 16, 397-405 (2011).
19. Thomson, J. A. et al. Isolation of a primate embryonic stem cell line. Proc. NatlAcad. Sci. USA 92, 7844-7848 (1995).
20. Sasaki, E. et al. Establishment of novel embryonic stem cell lines derivedfrom the common marmoset (Callithrix jacchus). Stem Cells 23, 1304-1313(2005).
21. Simerly, C. R. et al. Establishment and characterization of baboon embryonicstem cell lines: an Old World Primate model for regeneration andtransplantation research. Stem Cell Res. (Amst.) 2, 178-187 (2009).
22. Thomson, J. A. et al. Pluripotent cell lines derived from common marmoset(Callithrix jacchus) blastocysts. Biol. Reprod. 55, 254-259 (1996).
23. Thomson, J. A. et al. Embryonic stem cell lines derived from humanblastocysts. Science 282, 1145-1147 (1998).
24. Reubinoff, B. E., Pera, M. F., Fong, C. Y., Trounson, A. & Bongso, A. Embryonicstem cell lines from human blastocysts: somatic differentiation in vitro. Nat.Biotechnol. 18, 399-404 (2000).
25. Tachibana, M. et al. Generation of chimeric rhesus monkeys. Cell 148,285-295 (2012).
26. Simerly, C. et al. Interspecies chimera between primate embryonic stem cellsand mouse embryos: monkey ESCs engraft into mouse embryos, but notpost-implantation fetuses. Stem Cell Res. (Amst.) 7, 28-40 (2011).
27. James, D., Noggle, S. A., Swigut, T. & Brivanlou, A. H. Contribution ofhuman embryonic stem cells to mouse blastocysts. Dev. Biol. 295, 90-102(2006).
28. Nichols, J. & Smith, A. Naive and primed pluripotent states. Cell Stem Cell 4,487-492 (2009).
29. Boroviak, T., Loos, R., Bertone, P., Smith, A. & Nichols, J. The ability ofinner-cell-mass cells to self-renew as embryonic stem cells is acquiredfollowing epiblast specification. Nat. Cell Biol. 16, 516-528 (2014).
30. Brons, I. G. M. et al. Derivation of pluripotent epiblast stem cells frommammalian embryos. Nature 448, 191-195 (2007).
31. Tesar, P. J. et al. New cell lines from mouse epiblast share defining featureswith human embryonic stem cells. Nature 448, 196-199 (2007).
32. Huang, Y., Osorno, R., Tsakiridis, A. & Wilson, V. In vivo differentiation potentialof epiblast stem cells revealed by chimeric embryo formation. Cell Reports 2,1571-1578 (2012).
33. Kojima, Y. et al. The transcriptional and functional properties of mouse epiblaststem cells resemble the anterior primitive streak. Cell Stem Cell 14, 107-120(2014).
34. Wu, J. et al. An alternative pluripotent state confers interspecies chimaericcompetency. Nature 521, 316-321 (2015).
35. Mascetti, V. L. & Pedersen, R. A. Human-mouse chimerism validates humanstem cell pluripotency. Cell Stem Cell 18, 67-72 (2016).
36. Wu, J. & Izpisua Belmonte, J. C. Stem cells: a renaissance in human biologyresearch. Cell 165, 1572-1585 (2016).
37. Mascetti, V. L. & Pedersen, R. A. Contributions of mammalian chimeras topluripotent stem cell research. Cell Stem Cell 19, 163-175 (2016).
38. Hanna, J. et al. Human embryonic stem cells with biological and epigeneticcharacteristics similar to those of mouse ESCs. Proc. Natl Acad. Sci. USA 107,9222-9227 (2010).
39. Chan, Y.-S. et al. Induction of a human pluripotent state with distinct regulatorycircuitry that resembles preimplantation epiblast. Cell Stem Cell 13, 663-675(2013).
40. Duggal, G. et al. Alternative routes to induce naïve pluripotency in humanembryonic stem cells. Stem Cells 33, 2686-2698 (2015).
41. Gafni, O. et al. Derivation of novel human ground state naive pluripotent stemcells. Nature 504, 282-286 (2013).
42. Takashima, Y. et al. Resetting transcription factor control circuitry towardground-state pluripotency in human. Cell 158, 1254-1269 (2014).
43. Theunissen, T. W. et al. Systematic identification of culture conditions forinduction and maintenance of naive human pluripotency. Cell Stem Cell 15,471-487 (2014).
44. Theunissen, T. W. et al. Molecular criteria for defining the naive humanpluripotent state. Cell Stem Cell 19, 502-515 (2016).
45. Wang, J. et al. Primate-specific endogenous retrovirus-driven transcriptiondefines naive-like stem cells. Nature 516, 405-409 (2014).
46. Ware, C. B. et al. Derivation of naive human embryonic stem cells. Proc. NatlAcad. Sci. USA 111, 4484-4489 (2014).
47. Guo, G. et al. Naive pluripotent stem cells derived directly from isolated cells ofthe human inner cell mass. Stem Cell Rep. 6, 437-446 (2016).
48. Pera, M. F. In search of naivety. Cell Stem Cell 15, 543-545 (2014).
49. Huang, K., Maruyama, T. & Fan, G. The naive state of human pluripotent stemcells: a synthesis of stem cell and preimplantation embryo transcriptomeanalyses. Cell Stem Cell 15, 410-415 (2014).
50. Masaki, H. et al. Interspecific in vitro assay for the chimera-forming ability ofhuman pluripotent stem cells. Development 142, 3222-3230 (2015).
51. Chen, Y. et al. Generation of cynomolgus monkey chimeric fetuses usingembryonic stem cells. Cell Stem Cell 17, 116-124 (2015).
52. Fang, R. et al. Generation of naive induced pluripotent stem cells from rhesusmonkey fibroblasts. Cell Stem Cell 15, 488-496 (2014).
53. Dupin, E. & Sommer, L. Neural crest progenitors and stem cells: from earlydevelopment to adulthood. Dev. Biol. 366, 83-95 (2012).
54. Jaenisch, R. Mammalian neural crest cells participate in normal embryonicdevelopment on microinjection into post-implantation mouse embryos.Nature 318, 181-183 (1985).
55. Huszar, D., Sharpe, A. & Jaenisch, R. Migration and proliferation of culturedneural crest cells in W mutant neural crest chimeras. Development 112,131-141 (1991).
56. Cohen, M. A. et al. Human neural crest cells contribute to coat pigmentation ininterspecies chimeras after in utero injection into mouse embryos. Proc. NatlAcad. Sci. USA 113, 1570-1575 (2016).
57. Brüstle, O. et al. Chimeric brains generated by intraventricular transplantationof fetal human brain cells into embryonic rats. Nat. Biotechnol. 16, 1040-1044(1998).
58. Keyoung, H. M. et al. High-yield selection and extraction of two promoterdefinedphenotypes of neural stem cells from the fetal human brain. Nat.Biotechnol. 19, 843-850 (2001).
59. Goyama, S., Wunderlich, M. & Mulloy, J. C. Xenograft models for normal andmalignant stem cells. Blood 125, 2630-2640 (2015).
60. Zanjani, E. D., Almeida-Porada, G., Livingston, A. G., Flake, A. W. & Ogawa, M.Human bone marrow CD34? cells engraft in vivo and undergo multilineageexpression that includes giving rise to CD34+ cells. Exp. Hematol. 26, 353-360(1998).
61. Fujiki, Y. et al. Successful multilineage engraftment of human cord blood cellsin pigs after in utero transplantation. Transplantation 75, 916-922 (2003).
62. Muotri, A. R., Nakashima, K., Toni, N., Sandler, V. M. & Gage, F. H. Developmentof functional human embryonic stem cell-derived neurons in mouse brain.Proc. Natl Acad. Sci. USA 102, 18644-18648 (2005).
63. Chuma, S. et al. Spermatogenesis from epiblast and primordial germ cellsfollowing transplantation into postnatal mouse testis. Development 132,117-122 (2005).
64. Leitch, H. G. et al. On the fate of primordial germ cells injected into earlymouse embryos. Dev. Biol. 385, 155-159 (2014).
65. Clarke, D. L. et al. Generalized potential of adult neural stem cells. Science 288,1660-1663 (2000).
66. Jiang, Y. et al. Pluripotency of mesenchymal stem cells derived from adultmarrow. Nature 418, 41-49 (2002).
67. Geiger, H., Sick, S., Bonifer, C. & Müller, A. M. Globin gene expression isreprogrammed in chimeras generated by injecting adult hematopoietic stemcells into mouse blastocysts. Cell 93, 1055-1065 (1998).
68. Harder, F., Henschler, R., Junghahn, I., Lamers, M. C. & Müller, A. M. Humanhematopoiesis in murine embryos after injecting human cord blood-derivedhematopoietic stem cells into murine blastocysts. Blood 99, 719-721(2002).
69. Wilson, A. & Trumpp, A. Bone-marrow haematopoietic-stem-cell niches. Nat.Rev. Immunol. 6, 93-106 (2006).
70. Brinster, R. L. & Zimmermann, J. W. Spermatogenesis following malegerm-cell transplantation. Proc. Natl Acad. Sci. USA 91, 11298-11302 (1994).
71. Hayashi, K., Ohta, H., Kurimoto, K., Aramaki, S. & Saitou, M. Reconstitution ofthe mouse germ cell specification pathway in culture by pluripotent stemcells. Cell 146, 519-532 (2011).
72. Morata, G. & Ripoll, P. Minutes: mutants of Drosophila autonomously affectingcell division rate. Dev. Biol. 42, 211-221 (1975).
73. Amoyel, M. & Bach, E. A. Cell competition: how to eliminate your neighbours.Development 141, 988-1000 (2014).
74. Dejosez, M., Ura, H., Brandt, V. L. & Zwaka, T. P. Safeguards for cell cooperationin mouse embryogenesis shown by genome-wide cheater screen. Science341, 1511-1514 (2013).
75. Masaki, H. et al. Inhibition of apoptosis overcomes stage-related compatibilitybarriers to chimera formation in mouse embryos. Cell Stem Cell 19, 587-592(2016).
76. Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouseembryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676(2006).
77. Usui, J. et al. Generation of kidney from pluripotent stem cells via blastocystcomplementation. Am. J. Pathol. 180, 2417-2426 (2012).
78. Matsunari, H. et al. Blastocyst complementation generates exogenic pancreasin vivo in apancreatic cloned pigs. Proc. Natl Acad. Sci. USA 110, 4557-4562(2013).
79. Rashid, T., Kobayashi, T. & Nakauchi, H. Revisiting the flight of Icarus: makinghuman organs from PS cells with large animal chimeras. Cell Stem Cell 15,406-409 (2014).
80. Kobayashi, T., Kato-Itoh, M. & Nakauchi, H. Targeted organ generation usingMixl1-inducible mouse pluripotent stem cells in blastocyst complementation.Stem Cells Dev. 24, 182-189 (2015).
81. Li, Z. et al. 3D culture supports long-term expansion of mouse and humannephrogenic progenitors. Cell Stem Cell 19, 516-529 (2016).
82. Kuehn, M. R., Bradley, A., Robertson, E. J. & Evans, M. J. A potential animalmodel for Lesch-Nyhan syndrome through introduction of HPRT mutationsinto mice. Nature 326, 295-298 (1987).
83. Sen, S. Brownback. The Human Chimera Prohibition Act of 2005, S.659(109th Congress, 2005-2006).
84. Greely, H. T., Cho, M. K., Hogle, L. F. & Satz, D. M. Thinking about the humanneuron mouse. Am. J. Bioeth. 7, 27-40 (2007).
85. Hyun, I. et al. Ethical standards for human-to-animal chimera experiments instem cell research. Cell Stem Cell 1, 159-163 (2007).
86. Hermerén, G. Ethical considerations in chimera research. Development 142,3-5 (2015).
87. Hyun, I. From naïve pluripotency to chimeras: a new ethical challenge?Development 142, 6-8 (2015).
88. Robert, J. S. & Baylis, F. Crossing species boundaries. Am. J. Bioeth. 3, 1-13(2003).
89. Karpowicz, P., Cohen, C. B. & van der Kooy, D. It is ethical to transplant humanstem cells into nonhuman embryos. Nat. Med. 10, 331-335 (2004).
90. Karpowicz, P., Cohen, C. B. & van der Kooy, D. Developing human-nonhumanchimeras in human stem cell research: ethical issues and boundaries.Kennedy Inst. Ethics J. 15, 107-134 (2005).
91. Streiffer, R. in The Stanford Encyclopedia of Philosophy (ed. Zalta, E. N.)http://plato.stanford.edu/entries/chimeras/(2009).
92. Greely, H. T. in Oxford Handbook of Animal Ethics (eds Beauchamp, T. & Frey,R.G.) (Oxford Univ. Press, 2011).
93. Johnston, J. & Eliot, C. Chimeras and "human dignity". Am. J. Bioeth. 3, W6-W8(2003).
94. Palacios-González, C. Human dignity and the creation of human-nonhumanchimeras. Med. Health Care Philos. 18, 487-499 (2015).
95. United States National Institutes of Health. Special Notice: Moratorium onCertain Fetal Tissue Research. NIH Guide for Grants and Contracts. (Specialnotice, 8 May 1988).
96. United States National Institutes of Health Revitalization Act of 1993 PublicLaw 103-43 (1993).
97. Sherley v. Sebelius, 689 F.3d 776 (D.C. Circuit 2012).
98. Committee on Guidelines for Human Embryonic Stem Cell Research.Guidelines for Human Embryonic Stem Cell Research (National AcademiesPress, 2005).
99. International Society for Stem Cell Research. Guidelines for the Conduct ofHuman Embryonic Stem Cell Research http://www.isscr.org/home/publications/guide-clintrans (2006).
100. International Society for Stem Cell Research. Guidelines for Stem Cell Scienceand Clinical Translation http://www.isscr.org/home/publications/2016-guidelines (2016).
101. Academy of Medical Sciences. Animals Containing Human Materials https://issuu.com/acmedsci/docs/animals-containing-human-material. (2011).
102. Greene, M. et al. Ethics: moral issues of human-non-human primate neuralgrafting. Science 309, 385-386 (2005).
103. Palacios-González, C. Ethical aspects of creating human-nonhuman chimerascapable of human gamete production and human pregnancy. Monash Bioeth.Rev. 33, 181-202 (2015).
104. United States National Institutes of Health. NIH Research Involving Introductionof Human Pluripotent Cells into Non-Human Vertebrate Animal Pre-GastrulationEmbryos. https://grants.nih.gov/grants/guide/notice-files/NOT-OD-15-158.html (2015).
105. United States National Institutes of Health. Next Steps on Research UsingAnimal Embryos Containing Human Cells. http://osp.od.nih.gov/under-thepoliscope/2016/08/next-steps-research-using-animal-embryos-containinghuman-cells (2016).
106. Reardon, S. US agency to lift ban on funding human-animal hybrids. Nature536, 135 (2016).