Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1990 Jun 1;110(6):2087–2098. doi: 10.1083/jcb.110.6.2087

Distinct and different effects of the oncogenes v-myc and v-src on avian sympathetic neurons: retroviral transfer of v-myc stimulates neuronal proliferation whereas v-src transfer enhances neuronal differentiation

PMCID: PMC2116126  PMID: 2161856

Abstract

Immature avian sympathetic neurons are able to proliferate in culture for a limited number of divisions albeit expressing several neuron- specific properties. The effect of avian retroviral transfer of oncogenes on proliferation and differentiation of sympathetic neurons was investigated. Primary cultures of 6-d-old quail sympathetic ganglia, consisting of 90% neuronal cells, were infected by Myelocytomatosis virus (MC29), which contains the oncogene v-myc, and by the v-src-containing Rous sarcoma virus (RSV). RSV infection, in contrast to findings in other cellular systems, resulted in a reduction of neuronal proliferation as determined by 3H-thymidine incorporation (50% of control 4 d after infection) and in increased morphological differentiation. This is reflected by increased neurite production, cell size, and expression of neurofilament protein. In addition, RSV- infected neurons, unlike uninfected cells, are able to survive in culture for time periods up to 14 d in the absence of added neurotrophic factors. In contrast, retroviral transfer of v-myc stimulated the proliferation of immature sympathetic neurons preserving many properties of uninfected cells. The neuron-specific cell surface antigen Q211 and the adrenergic marker enzyme tyrosine hydroxylase were maintained in MC29-infected cells and in the presence of chick embryo extract the cells could be propagated over several weeks and five passages. Within 7 d after infection, the number of Q211-positive neurons increased approximately 100-fold. These data demonstrate distinct and different effects of v-src and v-myc-containing retroviruses on proliferation and differentiation of sympathetic neurons: v-src transfer results in increased differentiation, whereas v- myc transfer maintains an immature status reflected by proliferation, immature morphology, and complex growth requirements. The possibility of expanding immature neuronal populations by transfer of v-myc will be of considerable importance for the molecular analysis of neuronal proliferation and differentiation.

Full Text

The Full Text of this article is available as a PDF (3.5 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abrams H. D., Rohrschneider L. R., Eisenman R. N. Nuclear location of the putative transforming protein of avian myelocytomatosis virus. Cell. 1982 Jun;29(2):427–439. doi: 10.1016/0092-8674(82)90159-3. [DOI] [PubMed] [Google Scholar]
  2. Alemà S., Casalbore P., Agostini E., Tatò F. Differentiation of PC12 phaeochromocytoma cells induced by v-src oncogene. Nature. 1985 Aug 8;316(6028):557–559. doi: 10.1038/316557a0. [DOI] [PubMed] [Google Scholar]
  3. Anderson D. J., Axel R. A bipotential neuroendocrine precursor whose choice of cell fate is determined by NGF and glucocorticoids. Cell. 1986 Dec 26;47(6):1079–1090. doi: 10.1016/0092-8674(86)90823-8. [DOI] [PubMed] [Google Scholar]
  4. Bartlett P. F., Reid H. H., Bailey K. A., Bernard O. Immortalization of mouse neural precursor cells by the c-myc oncogene. Proc Natl Acad Sci U S A. 1988 May;85(9):3255–3259. doi: 10.1073/pnas.85.9.3255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bazill G. W., Haynes M., Garland J., Dexter T. M. Characterization and partial purification of a haemopoietic cell growth factor in WEHI-3 cell conditioned medium. Biochem J. 1983 Mar 15;210(3):747–759. doi: 10.1042/bj2100747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boettiger D., Roby K., Brumbaugh J., Biehl J., Holtzer H. Transformation of chicken embryo retinal melanoblasts by a temperature-sensitive mutant of Rous sarcoma virus. Cell. 1977 Aug;11(4):881–890. doi: 10.1016/0092-8674(77)90299-9. [DOI] [PubMed] [Google Scholar]
  7. Borasio G. D., John J., Wittinghofer A., Barde Y. A., Sendtner M., Heumann R. ras p21 protein promotes survival and fiber outgrowth of cultured embryonic neurons. Neuron. 1989 Jan;2(1):1087–1096. doi: 10.1016/0896-6273(89)90233-x. [DOI] [PubMed] [Google Scholar]
  8. Brackenbury R., Greenberg M. E., Edelman G. M. Phenotypic changes and loss of N-CAM-mediated adhesion in transformed embryonic chicken retinal cells. J Cell Biol. 1984 Dec;99(6):1944–1954. doi: 10.1083/jcb.99.6.1944. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  10. Brugge J. S., Cotton P. C., Queral A. E., Barrett J. N., Nonner D., Keane R. W. Neurones express high levels of a structurally modified, activated form of pp60c-src. Nature. 1985 Aug 8;316(6028):554–557. doi: 10.1038/316554a0. [DOI] [PubMed] [Google Scholar]
  11. Brugge J., Cotton P., Lustig A., Yonemoto W., Lipsich L., Coussens P., Barrett J. N., Nonner D., Keane R. W. Characterization of the altered form of the c-src gene product in neuronal cells. Genes Dev. 1987 May;1(3):287–296. doi: 10.1101/gad.1.3.287. [DOI] [PubMed] [Google Scholar]
  12. Bunte T., Donner P., Pfaff E., Reis B., Greiser-Wilke I., Schaller H., Moelling K. Inhibition of DNA binding of purified p55v-myc in vitro by antibodies against bacterially expressed myc protein and a synthetic peptide. EMBO J. 1984 Aug;3(8):1919–1924. doi: 10.1002/j.1460-2075.1984.tb02068.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Bunte T., Greiser-Wilke I., Donner P., Moelling K. Association of gag-myc proteins from avian myelocytomatosis virus wild-type and mutants with chromatin. EMBO J. 1982;1(8):919–927. doi: 10.1002/j.1460-2075.1982.tb01272.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Burnham P., Raiborn C., Varon S. Replacement of nerve-growth factor by ganglionic non-neuronal cells for the survival in vitro of dissociated ganglionic neurons. Proc Natl Acad Sci U S A. 1972 Dec;69(12):3556–3560. doi: 10.1073/pnas.69.12.3556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Campisi J., Gray H. E., Pardee A. B., Dean M., Sonenshein G. E. Cell-cycle control of c-myc but not c-ras expression is lost following chemical transformation. Cell. 1984 Feb;36(2):241–247. doi: 10.1016/0092-8674(84)90217-4. [DOI] [PubMed] [Google Scholar]
  16. Casalbore P., Agostini E., Alemà S., Falcone G., Tatò F. The v-myc oncogene is sufficient to induce growth transformation of chick neuroretina cells. Nature. 1987 Mar 12;326(6109):188–190. doi: 10.1038/326188a0. [DOI] [PubMed] [Google Scholar]
  17. Cotton P. C., Brugge J. S. Neural tissues express high levels of the cellular src gene product pp60c-src. Mol Cell Biol. 1983 Jun;3(6):1157–1162. doi: 10.1128/mcb.3.6.1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Crisanti P., Lorinet A. M., Calothy G., Pessac B. Glutamic acid decarboxylase activity is stimulated in quail retina neuronal cells transformed by Rous sarcoma virus and is regulated by pp60v-src. EMBO J. 1985 Jun;4(6):1467–1470. doi: 10.1002/j.1460-2075.1985.tb03804.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Denis N., Blanc S., Leibovitch M. P., Nicolaiew N., Dautry F., Raymondjean M., Kruh J., Kitzis A. c-myc oncogene expression inhibits the initiation of myogenic differentiation. Exp Cell Res. 1987 Sep;172(1):212–217. doi: 10.1016/0014-4827(87)90107-8. [DOI] [PubMed] [Google Scholar]
  20. DiCicco-Bloom E., Black I. B. Insulin growth factors regulate the mitotic cycle in cultured rat sympathetic neuroblasts. Proc Natl Acad Sci U S A. 1988 Jun;85(11):4066–4070. doi: 10.1073/pnas.85.11.4066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Donner P., Greiser-Wilke I., Moelling K. Nuclear localization and DNA binding of the transforming gene product of avian myelocytomatosis virus. Nature. 1982 Mar 18;296(5854):262–269. doi: 10.1038/296262a0. [DOI] [PubMed] [Google Scholar]
  22. Edgar D., Barde Y. A., Thoenen H. Subpopulations of cultured chick sympathetic neurones differ in their requirements for survival factors. Nature. 1981 Jan 22;289(5795):294–295. doi: 10.1038/289294a0. [DOI] [PubMed] [Google Scholar]
  23. Ernsberger U., Edgar D., Rohrer H. The survival of early chick sympathetic neurons in vitro is dependent on a suitable substrate but independent of NGF. Dev Biol. 1989 Oct;135(2):250–262. doi: 10.1016/0012-1606(89)90177-2. [DOI] [PubMed] [Google Scholar]
  24. Ernsberger U., Sendtner M., Rohrer H. Proliferation and differentiation of embryonic chick sympathetic neurons: effects of ciliary neurotrophic factor. Neuron. 1989 Mar;2(3):1275–1284. doi: 10.1016/0896-6273(89)90312-7. [DOI] [PubMed] [Google Scholar]
  25. Falcone G., Tatò F., Alemà S. Distinctive effects of the viral oncogenes myc, erb, fps, and src on the differentiation program of quail myogenic cells. Proc Natl Acad Sci U S A. 1985 Jan;82(2):426–430. doi: 10.1073/pnas.82.2.426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Fiszman M. Y., Fuchs P. Temperature-sensitive expression of differentiation in transformed myoblasts. Nature. 1975 Apr 3;254(5499):429–431. doi: 10.1038/254429a0. [DOI] [PubMed] [Google Scholar]
  27. Frederiksen K., Jat P. S., Valtz N., Levy D., McKay R. Immortalization of precursor cells from the mammalian CNS. Neuron. 1988 Aug;1(6):439–448. doi: 10.1016/0896-6273(88)90175-4. [DOI] [PubMed] [Google Scholar]
  28. Fults D. W., Towle A. C., Lauder J. M., Maness P. F. pp60c-src in the developing cerebellum. Mol Cell Biol. 1985 Jan;5(1):27–32. doi: 10.1128/mcb.5.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Gionti E., Pontarelli G., Cancedda R. Avian myelocytomatosis virus immortalizes differentiated quail chondrocytes. Proc Natl Acad Sci U S A. 1985 May;82(9):2756–2760. doi: 10.1073/pnas.82.9.2756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Graf T., Beug H. Avian leukemia viruses: interaction with their target cells in vivo and in vitro. Biochim Biophys Acta. 1978 Nov 17;516(3):269–299. doi: 10.1016/0304-419x(78)90011-2. [DOI] [PubMed] [Google Scholar]
  31. Howard M. J., Bronner-Fraser M. The influence of neural tube-derived factors on differentiation of neural crest cells in vitro. I. Histochemical study on the appearance of adrenergic cells. J Neurosci. 1985 Dec;5(12):3302–3309. doi: 10.1523/JNEUROSCI.05-12-03302.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Iba H., Jove R., Hanafusa H. Lack of induction of neuroretinal cell proliferation by Rous sarcoma virus variants that carry the c-src gene. Mol Cell Biol. 1985 Oct;5(10):2856–2859. doi: 10.1128/mcb.5.10.2856. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Iba H., Takeya T., Cross F. R., Hanafusa T., Hanafusa H. Rous sarcoma virus variants that carry the cellular src gene instead of the viral src gene cannot transform chicken embryo fibroblasts. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4424–4428. doi: 10.1073/pnas.81.14.4424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Jaffredo T., Vandenbunder B., Dieterlen-Lièvre F. In situ study of c-myc protein expression during avian development. Development. 1989 Apr;105(4):679–695. doi: 10.1242/dev.105.4.679. [DOI] [PubMed] [Google Scholar]
  35. Keane R. W., Lipsich L. A., Brugge J. S. Differentiation and transformation of neural plate cells. Dev Biol. 1984 May;103(1):38–52. doi: 10.1016/0012-1606(84)90005-8. [DOI] [PubMed] [Google Scholar]
  36. Krueger J. G., Garber E. A., Goldberg A. R. Subcellular localization of pp60src in RSV-transformed cells. Curr Top Microbiol Immunol. 1983;107:51–124. [PubMed] [Google Scholar]
  37. LEVI-MONTALCINI R., ANGELETTI P. U. Essential role of the nerve growth factor in the survival and maintenance of dissociated sensory and sympathetic embryonic nerve cells in vitro. Dev Biol. 1963 Mar;6:653–659. doi: 10.1016/0012-1606(63)90149-0. [DOI] [PubMed] [Google Scholar]
  38. Lachman H. M., Skoultchi A. I. Expression of c-myc changes during differentiation of mouse erythroleukaemia cells. Nature. 1984 Aug 16;310(5978):592–594. doi: 10.1038/310592a0. [DOI] [PubMed] [Google Scholar]
  39. Land H., Parada L. F., Weinberg R. A. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature. 1983 Aug 18;304(5927):596–602. doi: 10.1038/304596a0. [DOI] [PubMed] [Google Scholar]
  40. Leutz A., Beug H., Graf T. Purification and characterization of cMGF, a novel chicken myelomonocytic growth factor. EMBO J. 1984 Dec 20;3(13):3191–3197. doi: 10.1002/j.1460-2075.1984.tb02278.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Leutz A., Damm K., Sterneck E., Kowenz E., Ness S., Frank R., Gausepohl H., Pan Y. C., Smart J., Hayman M. Molecular cloning of the chicken myelomonocytic growth factor (cMGF) reveals relationship to interleukin 6 and granulocyte colony stimulating factor. EMBO J. 1989 Jan;8(1):175–181. doi: 10.1002/j.1460-2075.1989.tb03362.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Levy B. T., Sorge L. K., Meymandi A., Maness P. F. pp60c-src Kinase is in chick and human embryonic tissues. Dev Biol. 1984 Jul;104(1):9–17. doi: 10.1016/0012-1606(84)90031-9. [DOI] [PubMed] [Google Scholar]
  43. Lipsich L. A., Lewis A. J., Brugge J. S. Isolation of monoclonal antibodies that recognize the transforming proteins of avian sarcoma viruses. J Virol. 1983 Nov;48(2):352–360. doi: 10.1128/jvi.48.2.352-360.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Lynch S. A., Brugge J. S., Levine J. M. Induction of altered c-src product during neural differentiation of embryonal carcinoma cells. Science. 1986 Nov 14;234(4778):873–876. doi: 10.1126/science.3095923. [DOI] [PubMed] [Google Scholar]
  45. Maness P. F., Sorge L. K., Fults D. W. An early developmental phase of pp60c-src expression in the neural ectoderm. Dev Biol. 1986 Sep;117(1):83–89. doi: 10.1016/0012-1606(86)90350-7. [DOI] [PubMed] [Google Scholar]
  46. Martinez R., Mathey-Prevot B., Bernards A., Baltimore D. Neuronal pp60c-src contains a six-amino acid insertion relative to its non-neuronal counterpart. Science. 1987 Jul 24;237(4813):411–415. doi: 10.1126/science.2440106. [DOI] [PubMed] [Google Scholar]
  47. Maxwell G. D. Cell cycle changes during neural crest cell differentiation in vitro. Dev Biol. 1976 Mar;49(1):66–79. doi: 10.1016/0012-1606(76)90258-x. [DOI] [PubMed] [Google Scholar]
  48. Maxwell G. D., Sietz P. D. Development of cells containing catecholamines and somatostatin-like immunoreactivity in neural crest cultures: relationship of DNA synthesis to phenotypic expression. Dev Biol. 1985 Mar;108(1):203–209. doi: 10.1016/0012-1606(85)90023-5. [DOI] [PubMed] [Google Scholar]
  49. Ness S. A., Beug H., Graf T. v-myb dominance over v-myc in doubly transformed chick myelomonocytic cells. Cell. 1987 Oct 9;51(1):41–50. doi: 10.1016/0092-8674(87)90008-0. [DOI] [PubMed] [Google Scholar]
  50. Pacifici M., Boettiger D., Roby K., Holtzer H. Transformation of chondroblasts by Rous sarcoma virus and synthesis of the sulfated proteoglycan matrix. Cell. 1977 Aug;11(4):891–899. doi: 10.1016/0092-8674(77)90300-2. [DOI] [PubMed] [Google Scholar]
  51. Palmieri S., Kahn P., Graf T. Quail embryo fibroblasts transformed by four v-myc-containing virus isolates show enhanced proliferation but are non tumorigenic. EMBO J. 1983;2(12):2385–2389. doi: 10.1002/j.1460-2075.1983.tb01750.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Parker R. C., Varmus H. E., Bishop J. M. Expression of v-src and chicken c-src in rat cells demonstrates qualitative differences between pp60v-src and pp60c-src. Cell. 1984 May;37(1):131–139. doi: 10.1016/0092-8674(84)90308-8. [DOI] [PubMed] [Google Scholar]
  53. Pessac B., Girard A., Romey G., Crisanti P., Lorinet A. M., Calothy G. A neuronal clone derived from a Rous sarcoma virus-transformed quail embryo neuroretina established culture. Nature. 1983 Apr 14;302(5909):616–618. doi: 10.1038/302616a0. [DOI] [PubMed] [Google Scholar]
  54. Pessac B., Girard A., Romey G., Crisanti P., Wassef M., Privat A., Calothy G. Cells with neuronal properties in permanent cultures of quail embryo neuroretinas infected with Rous sarcoma virus. Brain Res. 1983 Sep 19;275(1):53–59. doi: 10.1016/0006-8993(83)90416-x. [DOI] [PubMed] [Google Scholar]
  55. Pessac B., Ziller C., Vautrin J., Girard A., Calothy G. Quail neural crest cells transformed by Rous sarcoma virus can be established into differentiating permanent cell cultures. Brain Res. 1985 Jun;352(2):235–239. doi: 10.1016/0165-3806(85)90110-5. [DOI] [PubMed] [Google Scholar]
  56. Reitsma P. H., Rothberg P. G., Astrin S. M., Trial J., Bar-Shavit Z., Hall A., Teitelbaum S. L., Kahn A. J. Regulation of myc gene expression in HL-60 leukaemia cells by a vitamin D metabolite. Nature. 1983 Dec 1;306(5942):492–494. doi: 10.1038/306492a0. [DOI] [PubMed] [Google Scholar]
  57. Resh M. D., Erikson R. L. Highly specific antibody to Rous sarcoma virus src gene product recognizes a novel population of pp60v-src and pp60c-src molecules. J Cell Biol. 1985 Feb;100(2):409–417. doi: 10.1083/jcb.100.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Rohrer H., Acheson A. L., Thibault J., Thoenen H. Developmental potential of quail dorsal root ganglion cells analyzed in vitro and in vivo. J Neurosci. 1986 Sep;6(9):2616–2624. doi: 10.1523/JNEUROSCI.06-09-02616.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Rohrer H., Hofer M., Hellweg R., Korsching S., Stehle A. D., Saadat S., Thoenen H. Antibodies against mouse nerve growth factor interfere in vivo with the development of avian sensory and sympathetic neurones. Development. 1988 Jul;103(3):545–552. doi: 10.1242/dev.103.3.545. [DOI] [PubMed] [Google Scholar]
  60. Rohrer H., Thoenen H. Relationship between differentiation and terminal mitosis: chick sensory and ciliary neurons differentiate after terminal mitosis of precursor cells, whereas sympathetic neurons continue to divide after differentiation. J Neurosci. 1987 Nov;7(11):3739–3748. doi: 10.1523/JNEUROSCI.07-11-03739.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Rohrschneider L. R. Immunofluorescence on avian sarcoma virus-transformed cells: localization of the src gene product. Cell. 1979 Jan;16(1):11–24. doi: 10.1016/0092-8674(79)90183-1. [DOI] [PubMed] [Google Scholar]
  62. Rothman T. P., Gershon M. D., Fontaine-Pérus J. C., Chanconie M., Le Douarin N. M. The effect of back-transplants of the embryonic gut wall on growth of the neural tube. Dev Biol. 1987 Dec;124(2):331–346. doi: 10.1016/0012-1606(87)90486-6. [DOI] [PubMed] [Google Scholar]
  63. Ruppert C., Goldowitz D., Wille W. Proto-oncogene c-myc is expressed in cerebellar neurons at different developmental stages. EMBO J. 1986 Aug;5(8):1897–1901. doi: 10.1002/j.1460-2075.1986.tb04442.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Rösner H., Al-Aqtum M., Henke-Fahle S. Developmental expression of GD3 and polysialogangliosides in embryonic chicken nervous tissue reacting with monoclonal antiganglioside antibodies. Brain Res. 1985 Feb;350(1-2):85–95. doi: 10.1016/0165-3806(85)90252-4. [DOI] [PubMed] [Google Scholar]
  65. Rösner H., Greis C., Henke-Fahle S. Developmental expression in embryonic rat and chicken brain of a polysialoganglioside-antigen reacting with the monoclonal antibody Q 211. Brain Res. 1988 Aug 1;470(2):161–171. doi: 10.1016/0165-3806(88)90234-9. [DOI] [PubMed] [Google Scholar]
  66. Schneider M. D., Perryman M. B., Payne P. A., Spizz G., Roberts R., Olson E. N. Autonomous expression of c-myc in BC3H1 cells partially inhibits but does not prevent myogenic differentiation. Mol Cell Biol. 1987 May;7(5):1973–1977. doi: 10.1128/mcb.7.5.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Shalloway D., Coussens P. M., Yaciuk P. Overexpression of the c-src protein does not induce transformation of NIH 3T3 cells. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7071–7075. doi: 10.1073/pnas.81.22.7071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Sorge L. K., Levy B. T., Maness P. F. pp60c-src is developmentally regulated in the neural retina. Cell. 1984 Feb;36(2):249–257. doi: 10.1016/0092-8674(84)90218-6. [DOI] [PubMed] [Google Scholar]
  69. Westin E. H., Wong-Staal F., Gelmann E. P., Dalla-Favera R., Papas T. S., Lautenberger J. A., Eva A., Reddy E. P., Tronick S. R., Aaronson S. A. Expression of cellular homologues of retroviral onc genes in human hematopoietic cells. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2490–2494. doi: 10.1073/pnas.79.8.2490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. ZACCHEI A. M. [The embryonal development of the Japanese quail (Coturnix coturnix japonica T. and S.)]. Arch Ital Anat Embriol. 1961;66:36–62. [PubMed] [Google Scholar]
  71. Ziller C., Fauquet M., Kalcheim C., Smith J., Le Douarin N. M. Cell lineages in peripheral nervous system ontogeny: medium-induced modulation of neuronal phenotypic expression in neural crest cell cultures. Dev Biol. 1987 Mar;120(1):101–111. doi: 10.1016/0012-1606(87)90108-4. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES