Development of adrenal chromaffin cells in Sf1 heterozygous mice
Tóm tắt
Adrenal medullary chromaffin cells are derivatives of the neural crest and are widely believed to share a common sympathoadrenal (SA) progenitor with sympathetic neurons. For decades, the adrenal cortical environment was assumed to be essential for channelling SA progenitors towards an endocrine chromaffin cell fate. Our recent analysis of steroidogenic factor 1(Sf1) −/− mice, which lack an adrenal cortex, has challenged this view: in Sf1 −/− mice chromaffin cells migrate to the correct “adrenal” location and undergo largely normal differentiation. In contrast to Sf1 homozygous mutants, heterozygous animals have an adrenal cortex, which, however, is smaller than in wildtype littermates. We show here that the Sf1 +/− adrenal cortical anlagen attract normal numbers of chromaffin progenitor cells into their vicinity by embryonic day 13.5 (E13.5). Two days later, however, only a few scattered cells with highly immature features have immigrated into the adrenal cortex, whereas the remainder form a coherent cell assembly ectopically located at the medial surface of the gland. These cells appear more mature than the scattered intracortical chromaffin progenitors and express the adrenaline synthesizing enzyme PNMT with a delay of 1 day in comparison with wildtype littermates. Nevertheless, chromaffin progenitor cells undergo a numerical reduction of approximately 30% by E17.5. Together, our data suggest that normal adrenocortical development is critical for the correct immigration of chromaffin progenitors into the cortical anlagen, for the timing of PNMT expression and for the regulation of chromaffin cell numbers.
Tài liệu tham khảo
Anderson DJ, Axel R (1986) A bipotential neuroendocrine precursor whose choice of cell fate is determined by NGF and glucocorticoids. Cell 47:1079–1090
Anderson DJ, Michelsohn A (1989) Role of glucocorticoids in the chromaffin-neuron developmental decision. Int J Dev Neurosci 12:83–94
Anderson DJ (1993) Molecular control of cell fate in the neural crest: the sympathoadrenal lineage. Annu Rev Neurosci 16:129–158
Bland ML, Fowkes RC, Ingraham HA (2004) Differential requirement for steroidogenic factor-1 gene dosage in adrenal development versus endocrine function. Mol Endocrinol 18:941–952
Bohn MC, Goldstein M, Black IB (1981) Role of glucocorticoids in expression of the adrenergic phenotype in rat embryonic adrenal gland. Dev Biol 82:1–10
Casarosa S, Fode C, Guillemot F (1999) Mash1 regulates neurogenesis in the ventral telencephalon.Development 126:525–534
Chester J, Phillips JC (1986) The adrenal and interrenal glands. In: Pang MP, Schreibman EC (eds) Vertebrates endocrinology: fundamentals and biomedical implications. Academic Press, New York, pp 319–350
Cole TJ, Blendy JA, Monaghan AP, Krieglstein K, Schmid W, Aguzzi A, Fantuzzi G, Hummler E, Unsicker K, Schutz G (1995) Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes Dev 13:1608–1621
Coupland RE (1965) The natural history of the chromaffin cell. Spottiswoode, Ballantyne, London Colchester
Coupland RE (1972) The chromaffin system. In: Blaschko H, Muscholl E (eds) Catecholamines. Handbook of Experimental Pharmacology, vol 33. Springer, Berlin Heidelberg New York, pp 16-45
Coupland RE, Tomlinson A (1989) The development and maturation of adrenal medullary chromaffin cells of the rat in vivo: a descriptive and quantitative study. Int J Dev Neurosci 7:419–438
Ernsberger U, Patzke H, Rohrer H (1997) The developmental expression of choline acetyltransferase (ChAT) and the neuropeptide VIP in chick sympathetic neurons: evidence for different regulatory events in cholinergic differentiation. Mech Dev 68:115–126
Ernsberger U, Esposito L, Partimo S, Huber K, Franke A, Bixby JL, Kalcheim C, Unsicker K (2005) Expression of neuronal markers suggests heterogeneity of chick sympathoadrenal cells prior to invasion of the adrenal anlagen. Cell Tissue Res 319:1–13
Finotto S, Krieglstein K, Schober A, Deimling F, Lindner K, Brühl B, Beier K, Metz J, Garcia-Arraras JE, Roig-Lopez JL, Monaghan P, Schmid W, Cole TJ, Kellendonk C, Tronche F, Schutz G, Unsicker K (1999) Analysis of mice carrying targeted mutations of the glucocorticoid receptor gene argues against an essential role of glucocorticoid signalling for generating adrenal chromaffin cells. Development 126:2935–2944
Guillemot F, Joyner AL (1993) Dynamic expression of the murine achaete-scute homologue mash-1 in the developing nervous system. Mech Dev 42:171–185
Gut P, Huber K, Lohr J, Bruhl B, Oberle S, Treier M, Ernsberger U, Kalcheim C, Unsicker K (2005) Lack of an adrenal cortex in Sf1 mutant mice is compatible with the generation and differentiation of chromaffin cells. Development 132:4611–4619
Huber K, Bruhl B, Guillemot F, Olson EN, Ernsberger U, Unsicker K (2002) Development of chromaffin cells depends on MASH1 function. Development 129:4729–4738
Lo LC, Johnson JE, Wuenschell CW, Saito T, Anderson DJ (1991) Mammalian achaete-scute homolog 1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. Genes Dev 5:1524–1537
Luo X, Ikeda Y, Parker KL (1994) A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 77:481–490
Matty AJ (1985) The adrenal and the kidney hormones. In: Matty AJ (ed) Fish endocrinology. Timber, Portland, pp 112–137
Michelsohn AM, Anderson DJ (1992) Changes in competence determine the timing of two sequential glucocorticoid effects on sympathoadrenal progenitors. Neuron 8:589–604
Orth DN, Kavacs WJ, Rowan DeBold C (1992) The adrenal cortex. In: Wilson JD, Foster DW (eds) William’s textbook of endocrinology. Saunders, Philadelphia, pp 489–619
Reissmann E, Ernsberger U, Francis-West PH, Rueger D, Brickell PM, Rohrer H (1996) Involvement of bone morphogenetic protein-4 and bone morphogenetic protein-7 in the differentiation of the adrenergic phenotype in developing sympathetic neurons. Development 122:2079–2088
Schneider C, Wicht H, Enderich J, Wegner M, Rohrer H (1999) Bone morphogenetic proteins are required in vivo for the generation of sympathetic neurons. Neuron 24:861–870
Shah AK, Lazatin J, Sinha RK, Lennox T, Hickok NJ, Tuan RS (1996) Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 85:331–343
Unsicker K (1993) The chromaffin cell: paradigm in cell, developmental, and growth factor biology. J Anat 183:207–221
Unsicker K, Krieglstein K (1996) Growth factors in chromaffin cells. Prog Neurobiol 48:307–324
Unsicker K, Huber K, Schutz G, Kalcheim C (2005) The chromaffin cell and its development. Neurochem Res 30:921–925
Wurtman RJ, Axelrod J (1966) Control of enzymatic synthesis of adrenaline in the adrenal medulla by adrenal cortical steroids. J Biol Chem 241:2301–2305
Yamamoto M, Yanai R, Arishima K (2004) Study of migration of neural crest cells to adrenal medulla by three-dimensional reconstruction. J Vet Med Sci 66:635–641
Zhou QY, Quaife CJ, Palmiter RD (1995) Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development. Nature 374:640–643