Establishment of SSEA-1- and Oct-4-expressing rat embryonic stem-like cell lines and effects of cytokines of the IL-6 family on clonal growth

Experimental Cell Research

Volumn 258, Issue 2, 2000, Pages 361-373

  Vassilieva, Svetlana ^a   Guan, Kaomei ^a   Pich, Uta ^a   Wobus, Anna M ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

Author keywords

Clonal growth; IL 6; LIF; Oct 4; Rat embryonic stem like cells; SSEA 1

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; CYTOKINE; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; LEUKEMIA INHIBITORY FACTOR; MESSENGER RNA; ONCOSTATIN M; STAGE SPECIFIC EMBRYO ANTIGEN 1; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CELL GROWTH; EMBRYO; EMBRYO CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; RAT; RNA ANALYSIS; STEM CELL;

ANIMALIA;

EID: 0034255655     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.2000.4940     Document Type: Article

References (80)

1. Wobus A. M., Holzhausen H., Jäkel P., Schöneich J. Characterization of a pluripotent stem cell line derived from a mouse embryo. Exp. Cell. Res. 152:1984;212-219.
2. Solter D., Knowles B. B. Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proc. Natl. Acad. Sci. USA. 75:1978;5565-5569.
3. Schöler H. R., Hatzopoulos A. K., Balling R., Suzuki N., Gruss P. A family of octamer specific proteins present during mouse embryogenesis: Evidence for germline-specific expression of an Oct factor. EMBO J. 8:1989;2543-2550.
4. Thomson J. A., Itskovitz-Eldor J., Shapiro S. S., Waknitz M. A., Swiergiel J. J., Marshall V. S., Jones M. J. Embryonic stem cell lines derived from human blastocysts. Science. 282:1998;1145-1147.
5. Rohwedel J., Sehlmeyer U., Shan J., Meister A., Wobus A. M. Primordial germ cell-derived mouse embryonic germ (EG) cells in vitro resemble undifferentiated stem cells with respect to differentiation capacity and cell cycle distribution. Cell. Biol. Int. 20:1996;579-587.
6. Bradley A., Evans M., Kaufman M. H., Robertson E. Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature. 309:1984;255-256.
7. Matsui Y., Zsebo K., Hogan B. L. Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell. 70:1992;841-847.
8. Resnick J. L., Bixler L. S., Cheng L., Donovan P. J. Long-term proliferation of mouse primordial germ cells in culture. Nature. 359:1992;550-551.
9. Stewart C. L., Gadi I., Bhatt H. Stem cells from primordial germ cells can reenter the germ line. Dev. Biol. 161:1994;626-628.
10. Labosky P. A., Barlow D. P., Hogan B. L. M. Embryonic germ cell lines and their derivation from mouse primordial germ cells. Ciba Found. Symp. 182:1994;157-178.
11. Collodi P., Kamei Y., Sharps A., Weber D., Barnes D. Fish embryo cell cultures for derivation of stem cells and transgenic chimeras. Mol. Mar. Biol. Biotechnol. 1:1992;257-265.
12. Sun L., Bradford C. S., Ghosh G., Collodi P. ES-like cell cultures derived from early zebrafish embryos. Mol. Mar. Biol. Biotechnol. 4:1995;193-199.
13. Hong Y., Winkler C., Schartl M. Pluripotency and differentiation of embryonic stem cell lines from the medakafish (Oryzias lapites). Mech. Dev. 60:1996;33-44.
14. Pain B., Clark M. E., Shen M., Nakazawa H., Sakura M., Samarut J., Etches R. J. Long-term in vitro culture and characterization of avian embryonic stem cells with multiple morphogenetic potentialities. Development. 122:1996;2339-2348.
15. Sukoyan M. A., Vatolin S. Y., Golubitsa A. N., Zhelezova A. I., Semenova L. A., Serov O. L. Embryonic stem cells derived from morulae, inner cell mass, and blastocysts of mink: comparisons of their pluripotencies. Mol. Reprod. Dev. 33:1993;148-158.
16. Doetschman T., Williams P., Maeda N. Establishment of hamster blastocyst-derived embryonic stem (ES) cells. Dev. Biol. 127:1988;224-227.
17. Graves K. H., Moreadith R. W. Derivation and characterization of putative pluripotential embryonic stem cells from preimplantation rabbit embryos. Mol. Reprod. Dev. 36:1993;424-433.
18. Wheeler M. B. Development and validation of swine embryonic stem cells: A review. Reprod. Fertil. Dev. 6:1994;563-568.
19. Notarianni E., Gall C., Laurie S., Moor R. M., Evans M. J. Derivation of pluripotent embryonic cell lines from the pig and sheep. J. Reprod. Fert. Suppl. 43:1991;255-260.
20. First N. L., Sims M. M., Park S. P., Kent-First M. J. Systems for production of calves from cultured bovine embryonic cells. Reprod. Fert. Dev. 6:1994;553-562.
21. Thomson J. A., Kalishman J., Golos T. G., Durning M., Harris C. P., Becker R. A., Hearn J. P. Isolation of a primate embryonic stem cell line. Proc. Natl. Acad. Sci. USA. 92:1995;7844-7848.
22. Thomson J. A., Kalishman J., Golos T. G., Durning M., Harris C. P., Hearn J. P. Pluripotent cell lines derived from Common Marmoset (Callithrix jacchus) blastocysts. Biol. Reprod. 55:1996;254-259.
23. Shamblott M. J., Axelman J., Wang S., Bugg E. M., Littlefield J. W., Donovan P. J., Blumenthal P. D., Huggins G. R., Gearhart J. D. Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc. Natl. Acad. Sci. USA. 95:1998;13726-13731.
24. Prelle K., Vassiliev I., Vassilieva S. G., Wolf E., Wobus A. M. Establishment of pluripotent cell lines from vertebrate species - present state and future prospects. Cell Tissues Organs. 165:1999;220-236.
25. Iannaccone P. M., Taborn G. U., Garton R. L., Caplice M. D., Brenin R. D. Pluripotent embryonic stem cells from the rat are capable of producing chimeras. Dev. Biol. 163:1994;288-292.
26. Ouhibi N., Sullivan N. F., English J., Colledge W. H., Evans M. J., Clark N. J. Initial culture behaviour of rat blastocysts on selected feeder cell lines. Mol. Reprod. Dev. 40:1995;311-324.
27. Stranzinger G. F. Embryonic stem cell-like cell lines of the specias rat and bovinae. Int. J. Exp. Path. 77:1996;263-267.
28. Brenin D., Look J., Bader M., Hübner N., Levan G., Iannaccone P. Rat embryonic stem cells: A progress report. Transplant Proc. 29:1997;1761-1765.
29. Smith A. G., Hooper M. L. Buffalo rat liver cells produce a diffusible activity wich inhibits the differentiation of murine embryonal carcinoma and embryonic stem cells. Dev. Biol. 121:1987;1-9.
30. Smith A. G., Heath J. K., Donaldson D. D., Wong G. G., Moreau J., Stahl M., Rogere D. Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature. 336:1988;688-690.
31. Williams R. L., Hilton D. J., Pease S., Willson T. A., Stewart C. L., Gearing D. P., Wagner E. F., Metcalf D., Nicola N. A., Gough N. M. Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature. 336:1988;684-687.
32. Baumann H., Zeigler S. F., Mosley B., Morella K. K, Pajovic S., Gearing D. P. Reconstitution of the response to leukemia inhibitory factor, oncostatin M, and ciliary neurotrophic factor in hepatoma cells. J. Biol. Chem. 268:1993;8414-8417.
33. Yamamori T., Fukada K., Aebersold R., Korsching S., Fann M. J., Patterson P. H. The cholinergic neuronal differentiation factor from heart cells is identical to leukaemia inhibitory factor. Science. 246:1989;1412-1416.
34. Leary A. G., Wong G. G., Clark S. C., Smith A. G., Ogawa M. Leukemia inhibitory factor differentiation-inhibiting activity/human interleukin for DA cells augments proliferation of human hematopoietic stem cells. Blood. 75:1990;1960-1964.
35. Musashi M., Clark S. C., Sudo T., Urdal D. L., Ogawa M. Synergistic interactions between interleukin-11 and interleukin-4 in support of proliferation of primitive hematopoietic progenitors of mice. Blood. 78:1991;1448-1451.
36. Conover I. C., Nancy Y. I., William T. P., Brian B., Mitchell P. G., DeChiara T. M., Yancopoulos G. D. Ciliary neurotrophic factor maintains the pluripotentiality of embryonic stem cells. Development. 119:1993;559-565.
37. Rose T. M., Weiford D. M., Gunderson N. L., Bruce A. G. Oncostatin M inhibits the differentiation of pluripotent embryonic stem cells in vitro. Cytokine. 6:1994;48-54.
38. Wolf E., Kramer R., Polejaeva I., Thoenen H., Brem G. Efficient generation of chimaeric mice using embryonic stem cells after long-term culture in the presence of ciliary neurotrophic factor. Transgenic Res. 3:1994;152-158.
39. Yoshida K., Chambers I., Nichols J., Smith A., Saito M., Yasukawa K., Shoyab M., Taga T., Kishimoto T. Maintenance of the pluripotential phenotype of embryonic stem cells through direct activation of gp130 signalling pathways. Mech. Dev. 45:1994;163-171.
40. Nichols J., Chambers I., Smith A. Derivation of germline competent embryonic stem cells with combination of interleukin-6 and soluble interleukin-6 receptor. Exp. Cell. Res. 215:1994;237-239.
41. Robertson E. J. Embryo-derived stem cell lines. Robertson E. J. Teratocarcinomas and Embryonic Stem Cells: A Practical Approach. 1987;71-112 IRL Press, Oxford.
42. Sehlmeyer U., Rohwedel J., Wobus A. M. Primordial germ cell-derived embryonic germ cells of the mouse - In vitro model for cytotoxicity studies with chemical mutagens. Toxicol. In Vitro. 10:1996;755-763.
43. Wong H., Andson W. D., Ting Cheng., Riabowol K. T. Monitoring mRNA expression by polymerase chain reaction: The "primer-dropping" method. Anal. Biochem. 223:1994;251-258.
44. Wobus A. M., Guan K., Shan J., Wellner M. C., Rohwedel J., Guanju J., Fleischmann B., Katus H A., Franz W. M. Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes. J. Mol. Cell. Cardiol. 29:1997;1525-1539.
45. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
46. Yeom Y. I., Fuhrmann G., Ovitt C. E., Brehm A., Ohbo K., Gross M., Hübner K., Schöler H. Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development. 122:1996;881-894.
47. Konecki D., Brennand J., Fuscoe J. C., Caskey C. T., Chinault A. C. Hypoxanthine-guanine phosphoribosyl-transferase genes of mouse and Chinese hamster: Construction and sequence analysis of cDNA recombinants. Nucleic Acids. Res. 10:1982;6763-6775.
48. Doetschman T. C., Eistetter H. R., Katz M., Schmidt W., Kemler R. The in vitro development of blastocyst-derived embryonic stem cell lines: Formation of visceral yolk sac, blood islands and myocardium. J. Embryol. Exp. Morphol. 87:1985;27-45.
49. Takahama Y., Ochiya T., Sasaki H., Baba-Toriyama H., Konishi H., Nakano H., Terada M. Molecular cloning and functional analysis of cDNA encoding a rat leukemia inhibitory factor: Towards generation of pluripotent rat embryonic stem cells. Oncogene. 16:1998;3189-3196.
50. Andrews P. W., Bronson D. L., Benham F., Strickland S., Knowles B. B. A comparative study of eight cell lines derived from human testicular teratocarcinoma. Cancer. 26:1980;269-280.
51. Strelchenko N. Bovine pluripotent stem cells. Theriogenology. 45:1996;131-140.
52. Cibelli J. B., Stice S. L., Golueke P. G., Kane J. J., Jerry J., Blackwell C., Ponce de Leon F., Robl J. M. Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science. 280:1998;1256-1258.
53. Van Stekelenburg-Hamers A. E. P., Van Achterberg T. A. E., Rebel H. G., Fleshon J. E., Campbell K. H. S., Weima S. M., Mummery C. L. Isolation and characterization of permanent cell lines from inner cell mass cells of bovine blastocyts. Mol. Reprod. Dev. 40:1995;444-454.
54. Pease S., Braghetta P., Gearing D., Grail D., Williams R. L. Isolation of embryonic stem (ES) cell lines in media supplemented with recombinant leukemia inhibitory factor (LIF). Dev. Biol. 141:1990;344-352.
55. Moens A., Flechon B., Degrouard J., Vignon X., Ding J., Flechon J. E., Betteridge K. J, Renard J. P. Ultrastructural and immunocytochemical analysis of diploid germ cells isolated from fetal rabbit gonads. Zygote. 5:1997;47-60.
56. Palmieri S. L., Peter W., Hess H., Schöler H. R. Oct-4 transcription factor is differentially expressed in the mouse embryo during establishment of the first two extraembryonic cell lineages involved in implantation. Dev. Biol. 166:1994;259-267.
57. Schöler H. R. Octamania: The POU factors in murine development. Trends Genet. 7:1991;323-329.
58. Pesce M., Anastassiadis K., Schöler H. R. Oct-4: Lessons of totipotency from embryonic stem cells. Cell Tissues Organs. 165:1999;144-152.
59. Nichols J., Zevnik B., Anastassiadis K., Niwa H., Klewe-Nebenius D., Chambers I., Schöler H., Smith A. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct-4. Cell. 95:1998;379-391.
60. Martin G. R. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. USA. 78:1981;7634-7638.
61. Gough N. M., Williams R. L., Hilton D. J., Pease S., Wilson T. A., Stahl J., Gearing D. P., Nicola N. A., Metcalf D. LIF: A molecule with divergent actions on myeloid leukaemic cells and embryonic stem cells. Reprod. Fertil. Dev. 1:1989;281-288.
62. Nichols J., Evans E. P., Smith A. G. Establishment of germ-line competent embryonic stem (ES) cells using differentiation inhibiting activity. Development. 110:1990;1341-1348.
63. Smith A. G. Culture and differentiation of embryonic stem cells. J. Tissue Culture Methods. 13:1991;84-94.
64. Taga T., Narazaki M., Yasukawa K., Saito T., Miki D., Hamaguchi M., Davis S., Shoyab M., Yancopoulos G. D., Kishimoto T. Functional inhibition of hematopoietic and neurotrophic cytokines by blocking the interleukin-6 signal transducer gp130. Proc. Natl. Acad. Sci. USA. 89:1992;10998-11001.
65. Akira S., Taga T., Kishimoto T. Interleukin-6 in biology and medicine. Adv. Immunol. 54:1993;1-78.
66. Paul S. R., Bennett F., Calvetti J. A., Kelleher K., Wood C. R., O'Hara R. M. Jr., Leary A. C., Sibley B., Clark S. C., Williams D. A., Yang Y.-C. Molecular cloning of cDNA encoding interleukin-11, a stromal cell-derived lymphopoietic and hematopoietic cytokine. Proc. Natl. Acad. Sci. USA. 87:1990;7512.
67. Pennica D., King K. L., Shaw K. J., Luis E., Rullamas J., Luoh S-M., Darbonne W. C., Knutzon D. S., Yen R., Chein K. R., Baker J. B., Wood W. I. Expression cloning of cardiotrophin-1, a cytokine that induces cardiac myocyte hypertrophy. Proc. Natl. Acad. Sci. USA. 92:1995;1142-1146.
68. Pennica D., Shaw K. J., Swanson T. A., Moor M. W., Shelton D. L., Zioncheck K. A., Rosenthal A., Taga T., Proni N. F., Wood W. I. Cardiotrophin-1. Biological activities and binding to the leukemia inhibitory factor receptor/gp 130 signaling complex. J. Biol. Chem. 270:1995;10915-10922.
69. Hara T., Tamura K., de Miguel M. P., Mukouyama Y., Kim H., Kogo H., Donovan P. J., Miyajima A. Distinct roles of Oncostatin M and leukemia inhibitory factor in the development of primordial germ cells and Sertoli cells in mice. Dev. Biol. 201:1998;144-153.
70. Mukouyama Y., Hara T., Xu M-J., Tamura K., Donovan P. J., Kim H-j., Kogo H., Tsuji K., Nakahata T., Miyajima A. In vitro expansion of murine multipotential hematopoietic progenitors from the embryonic aorta-gonad-mesonephros region. Immunity. 8:1998;105-114.
71. Taga T., Kishimoto T. Gp130 and the interleukin-6 family of cytokines. Annu. Rev. Immunol. 15:1997;797-819.
72. Murakami M., Hibi M., Nakagawa N., Nakagawa T., Yasukawa K., Yamanishi K., Taga T., Kishimoto T. IL-6 -induced homodimerization of gp130 and associated activation of a tyrosine kinase. Science. 260:1993;1808-1810.
73. Davis S., Aldrich T. H., Stahl N., Pan L., Taga T., Kishimoto T., Ip N. Y., Yancopoulos G. D. LIFR beta and gp130 as heterodimerizing signal transducers of the tripartite CNTF receptor. Science. 260:1993;1805-1808.
74. Stahl N., Farruggela J., Boulton T. G., Zhong Z., Darnell J. E., Yancopoulos C. D. Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science. 267:1995;1349-1353.
75. Starr R., Novak U., Willson T. A., Inglese M., Murphy V., Warren S. A., Metcalf D., Nicola A. N., Hilton D. J., Ernst M. Distinct roles for leukemia inhibitory factor receptor L-chain and gp130 in cell type-specific signal transduction. J. Biol. Chem. 32:1977;19982-19986.
76. Saito M., Yoshida K., Hibi M., Taga T., Kishimoto T. Molecular cloning of a murine IL-6 receptor-associated signal transduced, gp 130, and its regulated expression in vivo. J. Immunol. 148:1992;4066-4071.
77. Honda M., Yamamoto S., Chen M., Yasukawa K., Suzuki H., Saito T., Osugi Y., Tokunaga T., Kishimoto T. Human soluble IL-6 receptor; its detection and enhanced release by HIV infection. J. Immunol. 148:1992;2175-2180.
78. Suzuki H., Yasukawa K., Narazaki M., Hasegawa A., Taga T., Kishimoto T. Serum soluble interleukin-6 receptor in MRL/lpr mice is elevated with age and mediates the interleukin-6 signal. Eur. J. Immunol. 23:1993;1078-1082.
79. Dani C., Chambers I., Johnstone S., Robertson M., Ebrahimi B., Saito M., Taga T., Li M., Burdon T., Nichols J., Smith A. Paracrine induction of stem cell renewal by LIF-deficient cells: A new ES cell regulatory pathway. Dev. Biol. 203:1998;149-162.
80. Nagy A., Rossant J., Nagy R., Abramow-Newerly W., Roder J. C. Derivation of completely cell-culture-derived mice from early passage embryonic stem cells. Proc. Natl. Acad. Sci. USA. 90:1993;8424-8428.