mRNA expression patterns of the IGF system during mouse limb bud development, determined by whole mount in situ hybridization

Molecular and Cellular Endocrinology

Volumn 138, Issue 1-2, 1998, Pages 151-161

  Van Kleffens, Marjolein ^a   Groffen, Cora ^a   Rosato, Roberto R ^a   Van Den Eijnde, Stefan M ^b   Van Neck, Johan W ^a   Lindenbergh Kortleve, Dicky J ^a   Zwarthoff, Ellen C ^a   Drop, Stenvert L S ^a  

^a ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Apoptosis; Development; IGF; IGFBPs; Limb; Whole mount in situ hybridization

Indexed keywords

MESSENGER RNA; SOMATOMEDIN; SOMATOMEDIN B; SOMATOMEDIN BINDING PROTEIN; SOMATOMEDIN BINDING PROTEIN 2; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN BINDING PROTEIN 4; SOMATOMEDIN BINDING PROTEIN 5; SOMATOMEDIN C;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARTILAGE; CELL GROWTH; CHONDROGENESIS; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; IN SITU HYBRIDIZATION; JOINT; LIMB BUD; LIMB DEVELOPMENT; MESENCHYME; MOUSE; NONHUMAN; PHALANX; PRIORITY JOURNAL; TISSUE DIFFERENTIATION;

ANIMALS; CARTILAGE, ARTICULAR; CELL DIFFERENTIATION; EMBRYONIC AND FETAL DEVELOPMENT; FEMALE; FLUORESCENT DYES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; INSULIN-LIKE GROWTH FACTOR BINDING PROTEINS; INSULIN-LIKE GROWTH FACTOR I; INSULIN-LIKE GROWTH FACTOR II; JOINTS; LIMB BUD; MICE; MICE, INBRED BALB C; OXAZINES; PREGNANCY; RECEPTOR, IGF TYPE 1; RNA PROBES; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 0032536742     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0303-7207(98)00007-0     Document Type: Article

References (65)

1. Barth, J., Ivarie, R., 1994. Polyvinyl alcohol enhances detection of low abundance transcripts in early stage quail embryos in a nonradioactive whole mount in situ hybridization technique. Biotechniques 17, 324-327.
2. Charité, J., de Graaff, W., Shen, S., Deschamps, J., 1994. Ectopic expression of Hoxb-8 causes duplication of the ZPA in the fore limb and homeotic transformation of axial structures. Cell 78, 589-601.
3. Christofori, G., Naik, P., Hanahan, D., 1994. A second signal supplied by insulin-like growth factor II in oncogene-induced tumorigenesis. Nature 369, 414-417.
4. Chun, S., Billig, H., Tilly, J.L., Furuta, I., Tsafriri, A., Hsueh, A.J.W., 1994. Gonadotropin suppression of apoptosis in cultured preovulatory follicles: mediatory role of endogenous insulin-like growth factor I. Endocrinology 135, 1845-1853.
5. Coelho, C.N.D., Sumoy, L., Rodgers, B.J., Davidson, D.R., Hill, R.E., Upholt, W.B., Kosher, R.A., 1991. Expression of the chicken homeobox-containing gene Ghox-8 during embryonic chick limb development. Mech. Dev. 34, 143-154.
6. Cohn, M.J., Patel, K., Krumlauf, R., Wilkinson, D.G., Clarke, J.D., Tickle, C., 1997. Hox9 genes and vertebrate limb specification. Nature 387, 97-101.
7. Crossley, P.H., Minowada, G., MacArthur, C.A., Martin, G.R., 1996. Roles for FGF8 in the induction, initiation and maintenance of chick limb development. Cell 84, 127-136.
8. Daughaday, W.H., Hall, K., Raben, M.S., Salmon Jr, W.D., Van den Brande, J.L., Van Wyk, J.J., 1972. Somatomedin: proposed designation for sulphation factor. Nature 235, 107.
9. Dealy, C.N., Kosher, R.A., 1995. Studies on insulin-like growth factor-I and insulin in chick limb morphogenesis. Dev. Dyn. 202, 67-79.
10. Dealy, C.N., Kosher, R. A., 1996. IGF-I and insulin in the aquisition of limb-forming ability by the embryonic lateral plate. Dev. Biol. 177, 291-299.
11. Dealy, C.N., Clarke, K., Scranton, V., 1996. Ability of FGFs to promote the outgrowth and proliferation of limb mesoderm is dependent on IGF-I activity. Dev. Dyn. 206, 463-469.
12. Drop, S.L., Schuller, A.G., Lindenbergh-Kortleve, D.J., Groffen, C., Brinkman, A., Zwarthoff, E.C., 1992. Structural aspects of the IGFBP-family. Growth Regul. 2, 69-79.
13. Durham, S.K., De Leon, D.D., Okazaki, R., Riggs, B.L., Conover, C.A., 1995. Regulation of insulin-like growth factor (IGF) binding protein-4 availability in normal human osteoblast-like cells: role of endogenous IGFs. J. Clin. Endocrinol. Metab. 80, 104-110.
14. Francis, P.H., Richardson, M.K., Brickell, P.M., Tickle, C., 1994. Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb. Development 120, 209-218.
15. 3) limb buds: their relationships in the signalling cascade involved in limb patterning. Dev. Dyn. 203, 187-197.
16. Gabbitas, B., Pash, J., Canalis, E., 1994. Regulation of insulin-like growth factor-II synthesis in bone cell cultures by skeletal growth factors. Endocrinology 135, 284-289.
17. Gabbitas, B., Canalis, E., 1995. Bone morphogenetic protein-2 inhibits the synthesis of insulin-like growth factor binding protein-5 in bone cell cultures. Endocrinology 136, 2397-2403.
18. Gañan, Y., Macias, D., Duterque-Coquillaud, M., Ros, M.A., Hurle, J.M., 1996. Role of TGFβs and BMPs as signals controlling the position of the digits and the areas of interdigital cell death in the developing chick limb autopod. Development 122, 2349-2357.
19. Geduspan, J.S., Padanilam, B.J., Solursh, M., 1992. Coordinate expression of IGF-I and its receptor during limb outgrowth. Dev. Dyn. 195, 67-73.
20. Geduspan, J.S., Solursh, M., 1993. Effects of the mesonephros and insulin-like growth factor I on chondrogenesis of limb explants. Dev. Biol. 156, 500-508.
21. Hammerschmidt, M., Brook, A., Mcmahon, A.P., 1997. The world according to Hedgehog. Trends Genet. 13, 14-21.
22. Helder, M.N., Ozkaynak, E., Sampath, K.T., Luyten, F.P., Latin, V., Oppermann, H., Vukicevic, S., 1995. Expression pattern of osteogenic protein-1 (bone morphogenic protein-7) in human and mouse development. J. Histochem. Cytochem. 43, 1035-1044.
23. Helms, J.A., Kim, C.H., Eichele, G., Thaller, C., 1996. Retinoic acid signaling is required during early chick development. Development 122, 1385-1394.
24. Hurle, J.M., Gañan, Y., Macias, D., 1989. Experimental analysis of the in vivo chondrogenic potential of the interdidgital mesenchyme of the chick leg bud subjected to local ectodermal removal. Dev. Biol. 132, 368-374.
25. Hurle, J.M., Ros, M.A., Climent, V., Garcia-Martinez, V., 1996. Morphology and significance of programmed cell death in the developing limb bud of the vertebrate embryo. Micro Res. Tech. 34, 236-246.
26. Jones, J.I., Clemmons, D.R., 1995. Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 16, 3-34.
27. Kimura, S., Shiota, K., 1996. Sequential changes of programmed cell death in developing fetal mouse limbs and its possible roles in limb morphogenesis. J. Morphol. 229, 337-346.
28. Lau, M.M.H., Stewart, C.E.H., Liu, Z., Bhatt, H., Rotwein, P., Stewart, C.L., 1994. Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev. 8, 2953-2963.
29. Laufer, E., Nelson, C.E., Johnson, R.L., Morgan, B.A., Tabin, C., 1994. Sonic Hedgehog and Fgf-4 act through a signalling cascade and feedback loop to integrate growth and atterning of the developing limb bud. Cell 79, 993-1003.
30. Li, X.S., Chen, J.C., Sheikh, M.S., Shao, Z.M., Fontana, J.A., 1994. Retinoic acid inhibition of insulin-like growth factor-I stimulation of c-fos mRNA levels in a breast carcinoma cell line. Exp. Cell. Res. 211, 68-73.
31. Liu, L., Delbe, J., Blat, C., Zapf, J., Harel, L., 1992. Insulin-like growth factor binding protein-3 (IGFBP-3), an inhibitor of serum growth factors other than IGF-I and -II. J. Cell. Physiol. 153, 15-21.
32. Lyons, K.M., Pelton, R.W., Hogan, B.L.M., 1989. Patterns of expression of murine Vgr-1 and BMP-2a RNA suggest that transforming growth factor-β-like genes coordinately regulate aspects of embryonic development. Genes Dev. 3, 1657-1668.
33. Lyons, K.M., Pelton, R.W., Hogan, B.L., 1990. Organogenesis and pattern formation in the mouse; RNA distribution patterns suggest a role for bone morphogenetic protein-2A BMP-2A). Development 109, 833-844.
34. Macias, D., Gañan, Y., Ros, M.A., Hurle, J.M., 1996. In vivo inhibition of programmed cell death by local administration of FGF-2 and FGF-4 in the interdigital areas of the embryonic chick leg bud. Anat. Embryol. 193, 533-541.
35. Means, A.L., Gudas, L.J., 1995. The roles of retinoids in vertebrate development. Annu. Rev. Biochem. 64, 201-233.
36. Muragaki, Y., Mundlos, S., Upton, J., Olsen, B.R., 1996. Altered growth and branching patterns in synpolydactyly caused by mutations in HoxD13. Science 272, 548-551.
37. Oh, Y., Muller, H.L., Pham, H., Rosenfeld, R.G., 1993. Demonstration of receptors for insulin- like growth factor binding protein-3 on Hs578 human breast cells. J. Biol. Chem. 268, 26045-26048.
38. Paulsen, D.F., 1994. Retinoic acid in limb-bud outgrowth: review and hypothesis. Anat. Embryol. 190, 399-415.
39. Ralphs, J.R., Wylie, L., Hill, D.J., 1990. Distribution of insulin-like growth factor peptides in the developing chick embryo. Development 109, 51-58.
40. Resnicoff, M., Abraham, D., Yutanawiboonchai, W., Rotman, H.L., Kajstura, J., Rubin, R., Zoltick, P., Baserga, R., 1995. The insulin-like growth factor I receptor protects tumor cells from apoptosis in vivo. Cancer Res. 55, 2463-2469.
41. Ros, M.A., López-Martínez, A., Simandl, B.K., Rodriguez, C., Izpisúa-Belmonte, J.C., Dahn, R., Fallon, J., 1996. The limb field mesoderm determines initial limb bud antero-posterior asymmetry and the budding independent of sonic hedgehog or apical ectodermal gene expression. Development 122, 2319-2330.
42. Rosen, C.J., Donahue, L.R., Hunter, S.J., 1994. Insulin-like growth factors and bone: the osteoporosis connection. PSEBM 206, 83-102.
43. Ruberte, E., Friederich, V., Morriss-Kay, G., Chambon, P., 1992. Differential distribution patterns of CRABPI and CRABPII transcripts during mouse embryogenesis. Development 115, 973-987.
44. Saunders, J.W., Gasseling, M.T., 1968. Ectoderm-mesenchymal interactions in the origin of wing symmetry. In: Fleischmajer, R., Billingham, R.E. (Eds.), Epithelial-Mesenchymal Interactions. Williams & Wilkin, Baltimore, pp. 78-97.
45. Schofield, J.L., Wolpert, L., 1990. Effect of TGF-β1, TGF-β2 and bFGF on chick cartilage and muscle differentiation. Exp. Cell. Res. 191, 144-148.
46. Storm, E.E., Huynh, T.V., Copeland, N.G., Jenkins, N.A., Kingsley, D.M., Lee, S.-L., 1994. Limb alterations in brachypodism mice due to mutations in a new member of the TGF-beta superfamily. Nature 368, 639-643.
47. Storm, E.E., Kingsley, D.M., 1996. Joint patterning defects caused by single and double mutations in members of the bone morphogenetic protein (BMP) family. Development 122, 3969-3979.
48. Streck, R.D., Wood, T.L., Hsu, M-S., Pintar, J.E., 1992. Insulin-like growth factor I and II and insulin-like growth factor binding protein-2 RNAs are expressed in adjacent tissues within rat embryonic and fetal limbs. Dev. Biol. 151, 586-596.
49. Summerbell, D., 1974. A quantitative analysis of the effect of excision of the AER from the chick limb-bud. J. Embryol. Exp. Morphol. 32, 651-660.
50. Suzuki, H.R., Padanilam, B.J., Vitale, E., Ramirez, F., Solursh, M., 1991. Repeating developmental expression of G-Hox-7, a novel homeobox-containing gene in the chicken. Dev. Biol. 148, 375-388.
51. Theiler, K., 1972. The House Mouse. Springer, Berlin, Germany.
52. Tickle, C., 1996. Genetics and limb development. Dev. Genet. 19, 1-8.
53. Tonner, E., Quarrie, L., Travers, M., Barber, M., Logan, A., Wilde, C., Flint, D., 1995. Does an IGF-binding protein (IGFBP) present in involuting rat mammary gland regulate apoptosis? Prog. Growth Factor Res. 6, 409-414.
54. Ueda, K., Ganem, D., 1996. Apoptosis is induced by n-myc expression in hepatocytes, a frequent event in hepadnavirus oncogenesis, and is blocked by insulin-like growth factor II. J. Virol. 70, 1375-1383.
55. Wanek, N., Muneoka, K., Holler-Dinsmore, G., Burton, R., Bryant, S.V., 1989. A staging system for mouse limb development. J. Exp. Zool. 249, 41-49.
56. Wang, Z.-Q., Fung, M.R., Barlow, D.P., Wagner, E.F., 1994. Regulation of embryonic growth and lysosomal targeting by the imprinted Igf2/Mpr gene. Nature 372, 464-467.
57. White, E., 1996. Life, death, and the pursuit of apoptosis. Genes Dev. 10, 1-15.
58. Wilson, J.G., Roth, C.B., Warkany, J., 1953. An analysis of the syndrome of malformatios induced by maternal vitamin A deficiency: effects of restoration at various times during gestation. Am. J. Anat. 92, 189-217.
59. Woodward, T.L., Turner, J.D., Hung, H.T., Zhao, X., 1996. Inhibition of cellular proliferation and modulation of insulin-like growth factor binding proteins by retinoids in a bovine mammary epithelial cell line. J. Cell. Physiol. 167, 488-499.
60. Zakany, J., Duboule, D., 1996. Synpolydactyly in mice with targeted deficiency in the HoxD complex. Nature 384, 69-71.
61. Zakeri, Z.F., Quaglino, D., Latham, T., Lockshin, R.A., 1993. Delayed internucleosomal DNA fragmentation in programmed cell death. FASEB J. 7, 470-478.
62. Zakeri, Z., Quaglino, D., Singh Ahuja, H., 1994. Apoptotic cell death in the mouse limb and its suppression in the Hammertoe mutant. Dev. Biol. 165, 294-297.
63. Zhou, Y., Mohan, S., Linkhart, T.A., Baylink, D.J., Strong, D.D., 1996. Retinoic acid regulates insulin-like growth factor binding protein expression in human osteoblast cells. Endocrinology 137, 975-983.
64. Zou, H., Niswander, L., 1996. Requirement for BMP signaling in interdigital apoptosis and scale formation. Science 272, 738-741.
65. Zwilling, E., 1955. Ectoderm-mesoderm relationships in the development of the chick embryo limb bud. J. Exp. Zool. 128, 423-442.