The transcriptomes of novel marmoset monkey embryonic stem cell lines reflect distinct genomic features.

Katharina Debowski, Charis Drummer, Jana Lentes, Maren Cors, Ralf Dressel, Thomas Lingner, Gabriela Salinas-Riester, Sigrid Fuchs, Erika Sasaki, Rüdiger Behr
Author Information
  1. Katharina Debowski: Platform Degenerative Diseases, German Primate Center - Leibniz Institute for Primate Research, Kellnerweg 4, 37077 Göttingen, Germany.
  2. Charis Drummer: Platform Degenerative Diseases, German Primate Center - Leibniz Institute for Primate Research, Kellnerweg 4, 37077 Göttingen, Germany.
  3. Jana Lentes: Platform Degenerative Diseases, German Primate Center - Leibniz Institute for Primate Research, Kellnerweg 4, 37077 Göttingen, Germany.
  4. Maren Cors: Platform Degenerative Diseases, German Primate Center - Leibniz Institute for Primate Research, Kellnerweg 4, 37077 Göttingen, Germany.
  5. Ralf Dressel: Institute of Cellular and Molecular Immunology, University Medical Center Göttingen (UMG), Humboldtallee 34, 37073 Göttingen, Germany.
  6. Thomas Lingner: Microarray and Deep-Sequencing Core Facility, University Medical Center Göttingen (UMG), Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany.
  7. Gabriela Salinas-Riester: Microarray and Deep-Sequencing Core Facility, University Medical Center Göttingen (UMG), Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany.
  8. Sigrid Fuchs: Department of Human Genetics, University Medical Center Hamburg-Eppendorf, Martinistraße 52, 20246 Hamburg, Germany.
  9. Erika Sasaki: Department of Applied Developmental Biology, Central Institute for Experimental Animals, 3-25-12 Tonomachi Kawasaki-ku, Kawasaki, 210-0821 Japan.
  10. Rüdiger Behr: Platform Degenerative Diseases, German Primate Center - Leibniz Institute for Primate Research, Kellnerweg 4, 37077 Göttingen, Germany.

Abstract

Embryonic stem cells (ESCs) are useful for the study of embryonic development. However, since research on naturally conceived human embryos is limited, non-human primate (NHP) embryos and NHP ESCs represent an excellent alternative to the corresponding human entities. Though, ESC lines derived from naturally conceived NHP embryos are still very rare. Here, we report the generation and characterization of four novel ESC lines derived from natural preimplantation embryos of the common marmoset monkey (Callithrix jacchus). For the first time we document derivation of NHP ESCs derived from morula stages. We show that quantitative chromosome-wise transcriptome analyses precisely reflect trisomies present in both morula-derived ESC lines. We also demonstrate that the female ESC lines exhibit different states of X-inactivation which is impressively reflected by the abundance of the lncRNA X inactive-specific transcript (XIST). The novel marmoset ESC lines will promote basic primate embryo and ESC studies as well as preclinical testing of ESC-based regenerative approaches in NHP.

References

  1. Development. 2015 Jan 1;142(1):118-27 [PMID: 25480920]
  2. Nature. 2006 Nov 23;444(7118):481-5 [PMID: 16929302]
  3. Cell. 2012 Jan 20;148(1-2):285-95 [PMID: 22225614]
  4. Bioinformatics. 2015 Jan 15;31(2):166-9 [PMID: 25260700]
  5. Am J Med Genet. 1990 May;36(1):7-10 [PMID: 2185636]
  6. Neuroscience. 2012 Jun 1;211:13-27 [PMID: 22465440]
  7. Semin Fetal Neonatal Med. 2012 Dec;17(6):336-40 [PMID: 22871417]
  8. Stem Cells. 2006 Jun;24(6):1423-32 [PMID: 16543489]
  9. Nature. 2009 Aug 13;460(7257):863-8 [PMID: 19587682]
  10. Stem Cell Rev. 2014 Aug;10(4):472-9 [PMID: 24633531]
  11. Dev Dyn. 2001 Oct;222(2):273-9 [PMID: 11668604]
  12. Bioinformatics. 2005 Aug 15;21(16):3439-40 [PMID: 16082012]
  13. Genome Biol. 2010;11(10):R106 [PMID: 20979621]
  14. Science. 1998 Nov 6;282(5391):1145-7 [PMID: 9804556]
  15. Nature. 1981 Jul 9;292(5819):154-6 [PMID: 7242681]
  16. Nat Biotechnol. 2009 Nov;27(11):1033-7 [PMID: 19826408]
  17. Neurol Res. 2014 May;36(5):417-22 [PMID: 24649811]
  18. PLoS One. 2012;7(12):e52787 [PMID: 23300777]
  19. Cell Stem Cell. 2014 Nov 6;15(5):653-65 [PMID: 25517469]
  20. Curr Pharm Biotechnol. 2013;14(1):4-11 [PMID: 23092254]
  21. Bioinformatics. 2013 Jan 1;29(1):15-21 [PMID: 23104886]
  22. Mol Hum Reprod. 2015 Jan;21(1):66-80 [PMID: 25237007]
  23. PLoS One. 2010 Mar 08;5(3):e9580 [PMID: 20221450]
  24. EMBO J. 2015 Jul 2;34(13):1759-72 [PMID: 25908839]
  25. Hum Reprod. 2009 Jun;24(6):1359-72 [PMID: 19251728]
  26. Development. 2012 Dec;139(24):4514-23 [PMID: 23172912]
  27. Nat Commun. 2014 Oct 06;5:5042 [PMID: 25284313]
  28. Biochem Biophys Res Commun. 2013 Jun 14;435(4):551-6 [PMID: 23665319]
  29. Biol Reprod. 2004 Dec;71(6):1766-71 [PMID: 15128597]
  30. Stem Cells. 2005 Oct;23(9):1304-13 [PMID: 16109758]
  31. ILAR J. 2009;51(1):24-41 [PMID: 20075496]
  32. Cytogenet Cell Genet. 2001;94(3-4):206-15 [PMID: 11856883]
  33. Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7844-8 [PMID: 7544005]
  34. Stem Cells Transl Med. 2015 Jul;4(7):708-19 [PMID: 26019226]
  35. Development. 2015 Sep 15;142(18):3090-9 [PMID: 26395138]
  36. Bioinformatics. 2009 Aug 15;25(16):2078-9 [PMID: 19505943]
  37. Mol Aspects Med. 2012 Aug;33(4):487-509 [PMID: 22705444]
  38. Curr Opin Chem Biol. 2007 Aug;11(4):373-80 [PMID: 17681848]
  39. Cell Stem Cell. 2014 Feb 6;14(2):203-16 [PMID: 24506884]
  40. Dev Growth Differ. 2014 Jan;56(1):53-62 [PMID: 24387631]
  41. Genes Cells. 2010 Sep 1;15(9):959-69 [PMID: 20670273]
  42. Biol Reprod. 1996 Aug;55(2):254-9 [PMID: 8828827]
  43. Nat Rev Mol Cell Biol. 2016 Mar;17(3):155-69 [PMID: 26860365]
  44. Stem Cells Dev. 2011 Sep;20(9):1587-99 [PMID: 21126169]
  45. PLoS One. 2015 Mar 18;10(3):e0118424 [PMID: 25785453]
  46. Annu Rev Genet. 2008;42:733-72 [PMID: 18729722]
  47. Nature. 2002 Jul 4;418(6893):50-6 [PMID: 12077607]
  48. Stem Cells. 2015 Aug;33(8):2469-82 [PMID: 25982268]
  49. Am J Med Genet. 1996 Apr 24;62(4):330-5 [PMID: 8723059]
  50. Facts Views Vis Obgyn. 2011;3(1):15-21 [PMID: 24753843]
  51. Reproduction. 2012 May;143(5):597-609 [PMID: 22323619]
  52. Dev Cell. 2015 Nov 9;35(3):267-8 [PMID: 26555047]
  53. Stem Cells. 2005 Jun-Jul;23(6):805-16 [PMID: 15917476]
  54. Hum Genet. 1996 Mar;97(3):283-6 [PMID: 8786064]
  55. Hum Mol Genet. 2000 Jan 22;9(2):165-73 [PMID: 10607827]
  56. Nat Protoc. 2013 May;8(5):989-97 [PMID: 23619890]
  57. Nature. 2008 May 22;453(7194):519-23 [PMID: 18497825]
  58. Reproduction. 2013 Apr 15;145(4):439-51 [PMID: 23431271]
  59. Nature. 1996 Jan 11;379(6561):131-7 [PMID: 8538762]
  60. J Cell Sci. 2005 Oct 1;118(Pt 19):4495-509 [PMID: 16179608]
  61. Nat Med. 2009 May;15(5):577-83 [PMID: 19396175]
  62. Genomics. 1996 Apr 15;33(2):214-9 [PMID: 8660970]
  63. Dev Biol. 2004 Nov 15;275(2):403-21 [PMID: 15501227]
  64. Dev Cell. 2015 Nov 9;35(3):366-82 [PMID: 26555056]
  65. PLoS One. 2014 Dec 29;9(12 ):e116109 [PMID: 25546018]
  66. Theriogenology. 2012 Sep 1;78(4):811-6 [PMID: 22578624]
  67. Reprod Biomed Online. 2004 Dec;9(6):623-9 [PMID: 15670408]
  68. Genome Biol. 2010;11(2):R14 [PMID: 20132535]
  69. Am J Primatol. 2014 Sep;76(9):801-27 [PMID: 24723482]
  70. Cell Stem Cell. 2009 Jun 5;4(6):487-92 [PMID: 19497275]

MeSH Term

Animals
Biomarkers
Blastocyst
Callithrix
Cell Differentiation
Cell Line
Cell Shape
Embryonic Stem Cells
Female
Gene Expression Profiling
Gene Expression Regulation, Developmental
Genome
Karyotyping
Male
Morula
Sex Determination Processes
Teratoma
Transcriptome
X Chromosome Inactivation

Chemicals

Biomarkers