Visualisation of chicken macrophages using transgenic reporter genes: Insights into the development of the avian macrophage lineage

Development (Cambridge)

Volumn 141, Issue 16, 2014, Pages 3255-3265

  Balic, Adam ^a   Garcia Morales, Carla ^a   Vervelde, Lonneke ^a   Gilhooley, Hazel ^a   Sherman, Adrian ^a   Garceau, Valerie ^a   Gutowska, Maria W ^a   Burt, David W ^a   Kaiser, Pete ^a   Hume, David A ^a   Sang, Helen M ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Chicken; Dendritic cells; Embryonic development; Immunity; Macrophages; Transgenics

Indexed keywords

CHICKEN; DENDRITIC CELLS; EMBRYONIC DEVELOPMENT; IMMUNITY; MACROPHAGES; TRANSGENICS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; BIRDS; CELL LINEAGE; CHICKENS; DENDRITIC CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; GENETIC TECHNIQUES; IMMUNE SYSTEM; INTRONS; MACROPHAGES; MOLECULAR SEQUENCE DATA; PHAGOCYTOSIS; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; SEQUENCE HOMOLOGY, NUCLEIC ACID; SPECIES SPECIFICITY; TRANSGENES; YOLK SAC;

EID: 84905460397     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.105593     Document Type: Article

References (72)

1. Al-Roubaie, S., Hughe, J. H., Filla, M. B., Lansford, R., Lehoux, S. and Jones, E. A. V. (2012). Time-lapse microscopy of macrophages during embryonic vascular development. Dev. Dyn. 241, 1423-1431.
2. Auffray, C., Fogg, D., Garfa, M., Elain, G., Join-Lambert, O., Kayal, S., Sarnacki, S., Cumano, A., Lauvau, G. and Geissmann, F. (2007). Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317, 666-670.
3. Befus, A. D., Johnston, N., Leslie, G. A. and Bienenstock, J. (1980). Gutassociated lymphoid tissue in the chicken. I. Morphology, ontogeny, and some functional characteristics of Peyer's patches. J. Immunol. 125, 2626-2632.
4. Beug, H., von Kirchbach, A., Döderlein, G., Conscience, J.-F. and Graf, T. (1979). Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell 18, 375-390.
5. Bollerot, K., Romero, S., Dunon, D. and Jaffredo, T. (2005). Core binding factor in the early avian embryo: cloning of Cbfbeta and combinatorial expression patterns with Runx1. Gene Expr. Patterns 6, 29-39.
6. Brock, J., Midwinter, K., Lewis, J. and Martin, P. (1996). Healing of incisional wounds in the embryonic chick wing bud: characterization of the actin purse-string and demonstration of a requirement for Rho activation. J. Cell. Biol. 135, 1097-1107.
7. Burke, B., Ahmad, R., Staples, K. J., Snowden, R., Kadioglu, A., Frankenberger, M., Hume, D. A. and Ziegler-Heitbrock, L. (2008). Increased TNF expression in CD43++ murine blood monocytes. Immunol. Lett. 118, 142-147.
8. Casteleyn, C., Doom, M., Lambrechts, E., Van den Broeck, W., Simoens, P. and Cornillie, P. (2010). Locations of gut-associated lymphoid tissue in the 3-monthold chicken: a review. Avian Pathol. 39, 143-150.
9. Caxton-Martins, A. E. and Daimon, T. (1976). Histochemical observations on chicken blood and bone marrow cells. J. Anat. 122, 553-558.
10. Chapman, S. C., Collignon, J., Schoenwolf, G. C. and Lumsden, A. (2001). Improved method for chick whole-embryo culture using a filter paper carrier. Dev. Dyn. 220, 284-289.
11. Chitu, V. and Stanley, E. R. (2006). Colony-stimulating factor-1 in immunity and inflammation. Curr. Opin. Immunol. 18, 39-48.
12. Colucci-Guyon, E., Tinevez, J.-Y., Renshaw, S. A. and Herbomel, P. (2011). Strategies of professional phagocytes in vivo: unlike macrophages, neutrophils engulf only surface-associated microbes. J. Cell Sci. 124, 3053-3059.
13. Costa, R. M. B., Soto, X., Chen, Y., Zorn, A. M. and Amaya, E. (2008). spib is required for primitive myeloid development in Xenopus. Blood 112, 2287-2296.
14. Cuadros, M. A., Coltey, P., Carmen Nieto, M. and Martin, C. (1992). Demonstration of a phagocytic cell system belonging to the hemopoietic lineage and originating from the yolk sac in the early avian embryo. Development 115, 157-168.
15. Cuadros, M. A., Martin, C., Coltey, P., Almendros, A. and Navascués, J. (1993). First appearance, distribution, and origin of macrophages in the early development of the avian central nervous system. J. Comp. Neurol. 330, 113-129.
16. Cuadros, M. A., Santos, A. M., Martín-Oliva, D., Calvente, R., Tassi, M., Marín-Teva, J. L. and Navascués, J. (2006). Specific immunolabeling of brain macrophages and microglial cells in the developing and mature chick central nervous system. J. Histochem. Cytochem. 54, 727-738.
17. de Geus, E. D., Jansen, C. A. and Vervelde, L. (2012). Uptake of particulate antigens in a nonmammalian lung: phenotypic and functional characterization of avian respiratory phagocytes using bacterial or viral antigens. J. Immunol. 188, 4516-4526.
18. Del Cacho, E., Gallego, M., López-Bernard, F., Sánchez-Acedo, C. and Lillehoj, H. S. (2008). Isolation of chicken follicular dendritic cells. J. Immunol. Methods 334, 59-69.
19. Ebert, S., Weigelt, K., Walczak, Y., Drobnik, W., Mauerer, R., Hume, D. A., Weber, B. H. F. and Langmann, T. (2009). Docosahexaenoic acid attenuates microglial activation and delays early retinal degeneration. J. Neurochem. 110, 1863-1875.
20. Eikelenboom, P., Kroese, F. G. M. and van Rooijen, N. (1983). Immune complextrapping cells in the spleen of the chicken, enzyme histochemical and ultrastructural aspects. Cell Tissue Res. 231, 377-386.
21. Garceau, V., Smith, J., Paton, I. R., Davey, M., Fares, M. A., Sester, D.P., Burt, D.W. and Hume, D. A. (2010). Pivotal Advance: avian colony-stimulating factor 1 (CSF-1), interleukin-34 (IL-34), and CSF-1 receptor genes and gene products. J. Leukoc. Biol. 87, 753-764.
22. Garcia-Morales, C., Rothwell, L., Moffat, L., Garceau, V., Balic, A., Sang, H. M., Kaiser, P. and Hume, D. A. (2013). Production and characterisation of a monoclonal antibody that recognises the chicken CSF1 receptor and confirms that expression is restricted to macrophage-lineage cells. Dev. Comp. Immunol. 42, 278-285.
23. Hamburger, V. and Hamilton, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-92.
24. Herbomel, P., Thisse, B. and Thisse, C. (1999). Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126, 3735-3745.
25. Himes, S. R., Tagoh, H., Goonetilleke, N., Sasmono, T., Oceandy, D., Clark, R., Bonifer, C. and Hume, D. A. (2001). A highly conserved c-fms gene intronic element controls macrophage-specific and regulated expression. J. Leukoc. Biol. 70, 812-820.
26. Himly, M., Foster, D. N., Bottoli, I., Iacovoni, J. S. and Vogt, P. K. (1998). The DF-1 chicken fibroblast cell line: transformation induced by diverse oncogenes and cell death resulting from infection by avian leukosis viruses. Virology 248, 295-304.
27. Hopkinson-Woolley, J., Hughes, D., Gordon, S. and Martin, P. (1994). Macrophage recruitment during limb development and wound healing in the embryonic and foetal mouse. J. Cell Sci. 107, 1159-1167.
28. Houssaint, E. (1987). Cell lineage segregation during bursa of Fabricius ontogeny. J. Immunol. 138, 3626-3634.
29. Hume, D. A. (2006). The mononuclear phagocyte system. Curr. Opin. Immunol. 18, 49-53.
30. Hume, D. A. and MacDonald, K. P. A. (2012). Therapeutic applications of macrophage colony-stimulating factor-1 (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. Blood 119, 1810-1820.
31. Igyártó, B. Z., Lackó, E., Oláh, I. and Magyar, A. (2006). Characterization of chicken epidermal dendritic cells. Immunology 119, 278-288.
32. Igyártó, B. Z., Magyar, A. and Oláh, I. (2007). Origin of follicular dendritic cell in the chicken spleen. Cell Tissue Res. 327, 83-92.
33. Jeurissen, S. H. (1993). The role of various compartments in the chicken spleen during an antigen-specific humoral response. Immunology 80, 29-33.
34. Jeurissen, S. H. M., Janse, E. M., Kok, G. L. and De Boer, G. F. (1989). Distribution and function of non-lymphoid cells positive for monoclonal antibody CVI-ChNL-68.2 in healthy chickens and those infected with Marek's disease virus. Vet. Immunol. Immunopathol. 22, 123-133.
35. Jeurissen, S. H., Claassen, E. and Janse, E. M. (1992). Histological and functional differentiation of non-lymphoid cells in the chicken spleen. Immunology 77, 75-80.
36. Jones, C. V. and Ricardo, S. D. (2013). Macrophages and CSF-1: implications for development and beyond. Organogenesis 9, 249-260.
37. Kaufman, J., Salomonsen, J., Skjødt, K. and Thorpe, D. (1990). Size polymorphism of chicken major histocompatibility complex-encoded B-G molecules is due to length variation in the cytoplasmic heptad repeat region. Proc. Natl. Acad. Sci. USA 87, 8277-8281.
38. Le Douarin, N. M., Hallonet, M. E. R. and Pourquié, O. (1994). Cell migrations and establishment of neuronal connections in the developing brain: a study using the quail-chick chimera system. Prog. Brain. Res. 100, 3-18.
39. Li, L., Yan, B., Shi, Y.-Q., Zhang, W.-Q. and Wen, Z.-L. (2012). Live imaging reveals differing roles of macrophages and neutrophils during zebrafish tail fin regeneration. J. Biol. Chem. 287, 25353-25360.
40. Lichanska, A. M. and Hume, D. A. (2000). Origins and functions of phagocytes in the embryo. Exp. Hematol. 28, 601-611.
41. Lilja, H. E., Morrison, W. A., Han, X.-L., Palmer, J., Taylor, C., Tee, R., Möller, A., Thompson, E. W. and Abberton, K. M. (2013). An adipoinductive role of inflammation in adipose tissue engineering: key factors in the early development of engineered soft tissues. Stem Cells Dev. 22, 1602-1613.
42. MacDonald, K. P. A., Palmer, J. S., Cronau, S., Seppanen, E., Olver, S., Raffelt, N. C., Kuns, R., Pettit, A. R., Clouston, A., Wainwright, B. et al. (2010). An antibody against the colony-stimulating factor 1 receptor depletes the resident subset of monocytes and tissue-and tumor-associated macrophages but does not inhibit inflammation. Blood 116, 3955-3963.
43. Martín-Partido, G. and Navascués, J. (1990). Macrophage-like cells in the presumptive optic pathways in the floor of the diencephalon of the chick embryo. J. Neurocytol. 19, 820-832.
44. Martín-Partido, G., Cuadros, M. A., Martin, C., Coltey, P. and Navascués, J. (1991). Macrophage-like cells invading the suboptic necrotic centres of the avian embryo diencephalon originate from haemopoietic precursors. J. Neurocytol. 20, 962-968.
45. Mast, J., Goddeeris, B. M., Peeters, K., Vandesande, F. and Berghman, L. R. (1998). Characterisation of chicken monocytes, macrophages and interdigitating cells by the monoclonal antibody KUL01. Vet. Immunol. Immunopathol. 61, 343-357.
46. Mathias, J. R., Dodd, M. E., Walters, K. B., Yoo, S. K., Ranheim, E. A. and Huttenlocher, A. (2009). Characterization of zebrafish larval inflammatory macrophages. Dev. Comp. Immunol. 33, 1212-1217.
47. McCorkle, F. M., Stinson, R. S., Oláh, I. and Glick, B. (1979). The chicken's femoral-lymph nodules: T and B cells and the immune response. J. Immunol. 123, 667-669.
48. McGrew, M. J., Sherman, A., Ellard, F. M., Lillico, S. G., Gilhooley, H. J., Kingsman, A. J., Mitrophanous, K. A. and Sang, H. (2004). Efficient production of germline transgenic chickens using lentiviral vectors. EMBO Rep. 5, 728-733.
49. Mooney, J. E., Rolfe, B. E., Osborne, G. W., Sester, D. P., van Rooijen, N., Campbell, G. R., Hume, D. A. and Campbell, J. H. (2010). Cellular plasticity of inflammatory myeloid cells in the peritoneal foreign body response. Am. J. Pathol. 176, 369-380.
50. Nagy, N., Bíró, E., Takács, A., Pólos, M., Magyar, A. and Oláh, I. (2005). Peripheral blood fibrocytes contribute to the formation of the avian spleen. Dev. Dyn. 232, 55-66.
51. Nakamichi, Y., Udagawa, N. and Takahashi, N. (2013). IL-34 and CSF-1: similarities and differences. J. Bone Miner. Metab. 31, 486-495.
52. Oláh, I., Glick, B. and Taylor, R. L., Jr. (1984). Effect of soluble antigen on the ellipsoid-associated cells of the chicken's spleen. J. Leukoc. Biol. 35, 501-510.
53. Oláh, I., Kendall, C. and Glick, B. (1992). Anti-vimentin monoclonal antibody recognizes a cell with dendritic appearance in the chicken's bursa of Fabricius. Anat. Rec. 232, 121-125.
54. Ovchinnikov, D. A., DeBats, C. E. E., Sester, D. P., Sweet, M. J. and Hume, D. A. (2010). A conserved distal segment of the mouse CSF-1 receptor promoter is required for maximal expression of a reporter gene in macrophages and osteoclasts of transgenic mice. J. Leukoc. Biol. 87, 815-822.
55. Perry, M. M. (1988). A complete culture system for the chick embryo. Nature 331, 70-72.
56. Pollard, J.W. (2009). Trophic macrophages in development and disease. Nat. Rev. Immunol. 9, 259-270.
57. Pridans, C., Lillico, S., Whitelaw, B. and Hume, D. A. (2014). Lentiviral vectors containing mouse Csf1r control elements direct macrophage-restricted expression in multiple species of birds and mammals. Mol. Ther. Meth. Clin. Develop. 1, Article number: 14010.
58. Rotello, R. J., Fernandez, P. A. and Yuan, J. (1994). Anti-apogens and antiengulfens: monoclonal antibodies reveal specific antigens on apoptotic and engulfment cells during chicken embryonic development. Development 6, 1421-1431.
59. Sasmono, R. T., Oceandy, D., Pollard, J.W., Tong, W., Pavli, P., Wainwright, B. J., Ostrowski, M. C., Himes, S. R. and Hume, D. A. (2003). A macrophage colonystimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse. Blood 101, 1155-1163.
60. Sasmono, R. T., Ehrnsperger, A., Cronau, S. L., Ravasi, T., Kandane, R., Hickey, M. J., Cook, A. D., Himes, S. R., Hamilton, J. A. and Hume, D. A. (2007). Mouse neutrophilic granulocytes express mRNA encoding the macrophage colonystimulating factor receptor (CSF-1R) as well as many other macrophage-specific transcripts and can transdifferentiate into macrophages in vitro in response to CSF-1. J. Leukoc. Biol. 82, 111-123.
61. Sauka-Spengler, T. and Barembaum, M. (2008). Gain-and loss-of-function approaches in the chick embryo. Methods Cell Biol. 87, 237-256.
62. Sauter, K. A., Bouhlel, M. A., O'Neal, J., Sester, D. P., Tagoh, H., Ingram, R. M., Pridans, C., Bonifer, C. and Hume, D. A. (2013). The function of the conserved regulatory element within the second intron of the mammalian Csf1r locus. PLoS ONE 8, e54935.
63. Shaner, N. C., Lin, M. Z., McKeown, M. R., Steinbach, P. A., Hazelwood, K. L., Davidson, M. W. and Tsien, R. Y. (2008). Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat. Methods 5, 545-551.
64. Sherman, A., Dawson, A., Mather, C., Gilhooley, H., Li, Y., Mitchell, R., Finnegan, D. and Sang, H. (1998). Transposition of the Drosophila element mariner into the chicken germ line. Nat. Biotechnol. 16, 1050-1053.
65. Spurlin, J. W., III and Lwigale, P. Y. (2013). Wounded embryonic corneas exhibit nonfibrotic regeneration and complete innervation. Invest. Ophthalmol. Vis. Sci. 54, 6334-6344.
66. Stern, C. D. (2005). The chick; a great model system becomes even greater. Dev. Cell 8, 9-17.
67. Tagoh, H., Himes, R., Clarke, D., Leenen, P. J. M., Riggs, A. D., Hume, D. and Bonifer, C. (2002). Transcription factor complex formation and chromatin fine structure alterations at the murine c-fms (CSF-1 receptor) locus during maturation of myeloid precursor cells. Genes Dev. 16, 1721-1737.
68. Underhill, D. M. (2003). Macrophage recognition of zymosan particles. J. Endotoxin Res. 9, 176-180.
69. Vaughn, L. E., Holt, P. S., Moore, R. W. and Gast, R. K. (2006). Enhanced gross visualization of chicken Peyer's patch: novel staining technique applied to fresh tissue specimens. Avian Dis. 50, 298-302.
70. Wang, T., Kono, T., Monte, M. M., Kuse, H., Costa, M. M., Korenaga, H., Maehr, T., Husain, M., Sakai, M. and Secombes, C. J. (2013). Identification of IL-34 in teleost fish: differential expression of rainbow trout IL-34, MCSF1 and MCSF2, ligands of the MCSF receptor. Mol. Immunol. 53, 398-409.
71. Wong, K. L., Yeap, W. H., Tai, J. J. Y., Ong, S. M., Dang, T. M. and Wong, S. C. (2012). The three human monocyte subsets: implications for health and disease. Immunol. Res. 53, 41-57.
72. Wynn, T. A., Chawla, A. and Pollard, J. W. (2013). Macrophage biology in development, homeostasis and disease. Nature 496, 445-455.