Cell Loss and Autophagy in the Extra-Adrenal Chromaffin Organ of Zuckerkandl are Regulated by Glucocorticoid Signalling

Journal of Neuroendocrinology

Volumn 25, Issue 1, 2013, Pages 34-47

  Schober, Andreas ^a   Parlato, Rosanna ^b   Huber, Katrin ^a   Kinscherf, Ralf ^c   Hartleben, Björn ^d   Huber, Tobias B ^a,d   Schütz, Günther ^b   Unsicker, Klaus ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b GERMAN CANCER RESEARCH CENTER   (Germany)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Atg5 deficient mice; Autophagic cell death; Conditional deletion; Glucocorticoid receptor; Neuroendocrine chromaffin cells

Indexed keywords

AUTOPHAGY PROTEIN 5; CATHEPSIN D; DOPAMINE BETA MONOOXYGENASE; GLUCOCORTICOID RECEPTOR; PROTEIN P62;

ADRENAL GLAND; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOLYSOSOME; AUTOPHAGY; CELL LOSS; CELL VACUOLE; CHROMAFFIN CELL; CONTROLLED STUDY; ELECTRON MICROSCOPY; FEMALE; GENE DELETION; GENE EXPRESSION; MACROPHAGE; MOUSE; NONHUMAN; ORGAN OF ZUCKERKANDL; PRIORITY JOURNAL;

ANIMALS; AUTOPHAGY; CASPASE 3; CATHEPSIN D; CELL COUNT; CHROMAFFIN CELLS; GENE KNOCKDOWN TECHNIQUES; GLUCOCORTICOIDS; MICE; PARA-AORTIC BODIES; RECEPTORS, GLUCOCORTICOID; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84871504893     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2012.02367.x     Document Type: Article

References (75)

1. Unsicker K, Stahnke G, Müler TH. Survival, morphology, and catecholamine storage of chromaffin cells serum-free culture: evidence for a survival and differentiation promoting activity in medium conditioned by purified chromaffin cells. Neurochem Res 1987; 12: 995-1003.
2. Unsicker K, Huber K, Schütz G, Kalcheim C. The chromaffin cell and its development. Neurochem Res 2005; 30: 921-925.
3. Böck P. The Paraganglia. In: Oksche A & Vollrath L, ed. Handbuch der mikroskopischen Anatomie des Menschen. Volume VI, Part 8. Berlin: Springer, 1982.
4. Coupland RE. The natural history of the chromaffin cell. London: Longmans, Green and Co., 1965.
5. Kohn A. Die Paraganglien. Arch Mikrosk Anat 1903; 52: 262-365.
6. Zuckerkandl E. Ueber Nebenorgane des Sympathicus im Retroperitoneal-raum des Menschen. Verh Anat Ges 1901; 15: 95-107.
7. West GB, Shepard DM, Hunter RB, McGregor AR. The function of the organs of Zuckerkandl. Clin Sci Lond 1953; 12: 317-325.
8. Fitzgerald RS, Eyzaguirre C, Zapata P. Fifty years of progress in carotid body physiology. Adv Exp Med Biol 2009; 648: 19-28.
9. Hervonen A, Vaalasti A, Partanen M, Kanerva L, Vaalasti T. The paraganglia, a persisting endocrine system in man. Am J Anat 1976; 146: 207-210.
10. Lahiri S, Nishino T, Mokashi A, Mulligan E. Relative responses of aortic body and carotid body chemoreceptors to hypotension. J Appl Physiol 1980; 48: 781-788.
11. Prabhakar NR, Peng YJ. Pripheral chemoreceptors in health and disease. J Appl Physiol 2004; 96: 359-366.
12. de Gallardo MR, Freire F, Hogan L, Tramezzani JH. The organ of Zuckerkandl of the golden hamster (Mesocricetus auratus). Gen Comp Endocrinol 1974; 22: 507-18.
13. de Gallardo MR, Freire F, Tramezzani JH. The organ of Zuckerkandl of the newborn rat and its postnatal involution. Acta Physiol Lat Am 1974; 24: 290-304.
14. Goormaghtigh N. Les glandes annexes du système nervouxes autonome (note préliminaire). Brux Méd 1935; 16: 38-44.
15. Iwanow G. Zur Frage der Genese und Reduktion der Paraganglien des Menschen. Z Ges Anat 1. Z Anat EntwGesch 1925; 77: 234-244.
16. Ober WB. Emil Zuckerkandl and his delightful little organ. Pathol Annu 1983; 1: 103-119.
17. Subramanian A, Maker VK. Organs of Zuckerkandl: their surgical significance and a review of a century of literature. Am J Surg 2006; 192: 224-234.
18. Espejo EF, Gonzalez-Albo MC, Moraes JP, El Banoua F, Flores JA, Caraballo I. Functional regeneration in a rat Parkinson's model after intrastriatal grafts of glial cell line-derived neurotrophic factor and transforming growth factor beta1-expressing extra-adrenal chromaffin cells of the Zuckerkandl's organ. J Neurosci 2001; 2: 9888-9895.
19. Galan-Rodriguez B, del-Marco A, Flores JA, Ramiro-Fuentes S, Gonzalez-Aparicio R, Tunez I, Tasset I, Fernandez-Espejo E. Grafts of extra-adrenal chromaffin cells as aggregates show better survival rate and regenerative effects on parkinsonian rats than dispersed cell grafts. Neurobiol Dis 2008; 29: 529-542.
20. Wurtman RJ, Axelrod J. Adrenaline synthesis: control by the pituitary gland and adrenal glucocorticoids. Science 1965; 150: 1464-1465.
21. Anderson DJ, Axel R. A bipotential neuroendocrine precursor whose choice of cell fate is determined by NGF and glucocorticoids. Cell 1986; 47: 1079-1090.
22. Unsicker K, Krisch B, Otten U, Thoenen H. Nerve growth factor-induced fiber outgrowth from isolated rat adrenal chromaffin cells: impairment by glucocorticoids. Proc Natl Acad Sci USA 1978; 75: 3498-3502.
23. 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, Schütz G, Unsicker K. 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 1999; 126: 2935-2944.
24. Parlato R, Otto C, Tuckermann J, Stotz S, Kaden S, Gröne HJ, Unsicker K, Schütz G. Conditional inactivation of glucocorticoid receptor gene in dopamine-beta-hydroxylase cells impairs chromaffin cell survival. Endocrinology 2009; 150: 1775-1781.
25. Eränkö O, Lempinen M, Räisänen L. Adrenaline and noradrenaline in the organ of Zuckerkandl and adrenals of newborn rats treated with hydrocortisone. Acta Physiol Scand 1966; 66: 253-254.
26. Eränkö L. The practical histochemical demonstration of catecholamines by formaldehyde-induced fluorescence. J R Micr Soc 1967; 87: 259-276.
27. Lempinen M. Effect of cortisone on extra-adrenal chromaffin tissue of the rat. Nature 1963; 199: 74-75.
28. Monkhouse WS, Coupland RE. The effect of in vivo hydrocortisone administration on the labelling index and size of the intra- and extra-adrenal chromaffin tissue of the fetal and perinatal mouse. J Anat 1985; 140: 679-696.
29. Monkhouse WS. The effect of in vivo hydrocortisone administration on the labelling index and size of chromaffin tissue in the postnatal and adult mouse. J Anat 1986; 144: 133-144.
30. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006; 41: 885-889.
31. Schober A, Minichiello L, Keller M, Huber K, Layer PG, Roig-López JL, García-Arrarás JE, Klein R, Unsicker K. Reduced acetylcholinesterase (AChE) activity in adrenal medulla and loss of sympathetic preganglionic neurons in TrkA-deficient, but not TrkB-deficient, mice. J Neurosci 1997; 17: 891-903.
32. Ernsberger U, Patzke H, Rohrer H. 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 1997; 68: 115-126.
33. Huber K, Brühl B, Guillemot F, Olson EN, Ernsberger U, Unsicker K. Development of chromaffin cells depend on MASH1 funktion. Development 2002; 129: 4729-4738.
34. Pohlmann R, Boeker MW, von Figura K. The two mannose 6-phosphate receptors transport distinct complements of lysosomal proteins. J Biol Chem 1995; 270: 27311-27318.
35. Hartleben B, Gödel M, Meyer-Schwesinger C, Liu S, Ulrich T, Köbler S, Wiech T, Grahammer F, Arnold SJ, Lindenmeyer MT, Cohen CD, Pavenstädt H, Kerjaschki D, Mizushima N, Shaw AS, Walz G, Huber TB. Autophagy influences glomerular disease susceptibility and maintains podocyte homeostasis in aging mice. J Clin Invest 2010; 120: 1084-1096.
36. Roosen A, Schober A, Strelau J, Bottner M, Faulhaber J, Bendner G, McIlwrath SL, Seller H, Ehmke H, Lewin GR, Unsicker K. Lack of neurotrophin-4 causes selective structural and chemical deficits in sympathetic ganglia and their preganglionic innervation. J Neurosci 2001; 21: 3073-3084.
37. Hedreen JC. Lost caps in histological counting methods. Anat Rec 1998; 250: 366-372.
38. Schober A, Peterziel H, von Bartheld CS, Simon H, Krieglstein K, Unsicker K. GDNF applied to the MPTP-lesioned nigrostriatal system requires TGF-beta for its neuroprotective action. Neurobiol Dis 2007; 25: 378-391.
39. von Bartheld CS. Counting particles in tissue sections: choices of methods and importance of calibration to minimize biases. Histol Histopathol 2002; 17: 639-648.
40. Disick GI, Palese MA. Extra-adrenal pheochromocytoma: diagnosis and management. Curr Urol Rep 2007; 8: 83-88.
41. Falck B, Hillarp NA, Thieme G, Torp A. Fluorescence of catechol amines and related compounds condensed with formaldehyde. Brain Res Bull 1982; 9: 11-15.
42. Itakura E, Mizushima N. Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy 2010; 6: 764-776.
43. Klionsky DJ, Cuervo AM, Seglen PO. Methods for monitoring autophagy from yeast to human. Autophagy 2007; 3: 181-206.
44. Komatsu M, Ichimura Y. Physiological significance of selective degradation of p62 by autophagy. FEBS Lett 2010; 584: 1374-1378.
45. Bjørkøy G, Lamark T, Pankiv S, Øvervatn A, Brech A, Johansen T. Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol 2009; 452: 181-197.
46. Taatjes DJ, Sobel BE, Budd RC. Morphological and cytochemical determination of cell death by apoptosis. Histochem Cell Biol 2008; 129: 33-43.
47. Brundin T. Storage and in vitro release rate of catecholamines from granules isolated from preaortal paraganglia and adrenals of newborn rabbits. Acta Physiol Scand 1966a; 66: 406-409.
48. Hervonen A, Korkala O. The effect of hypoxia on the catecholamine content of human fetal abdominal paraganglia and adrenal medulla. Acta Obstet Gynecol Scand 1972; 51: 17-24.
49. Hervonen A, Korkala O. Effect of hypoxia on the fine structure of the catecholamine-storing cells of the human fetal paraganglia. Virchows Arch B Cell Pathol 1973; 13: 341-349.
50. Dalle M, Giry J, Gay M, Delost P. Perinatal changes in plasma and adrenal corticosterone and aldosterone concentrations in the mouse. J Endocrinol 1978; 76: 303-309.
51. Henning SJ. Plasma concentrations of total and free corticosterone during development in the rat. Am J Physiol 1978; 235: 451-456.
52. Erdmann G, Schütz G, Berger S. Loss of glucocorticoid receptor function in the pituitary results in early postnatal lethality. Endocrinology 2008; 149: 3446-3451.
53. Schmidt MV, Enthoven L, van der Mark M, Levine S, de Kloet ER, Oitzl MS. The postnatal development of the hypothalamic-pituitary-adrenal axis in the mouse. Int J Dev Neurosci 2003; 21: 125-132.
54. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451: 1069-1075.
55. Mizushima N, Levine B. Autophagy in mammalian development and differentiation. Nat Cell Biol 2010; 12: 823-830.
56. Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol 2010a; 12: 814-822.
57. Yang Z, Klionsky DJ. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol 2010b; 22: 124-131.
58. Longatti A, Tooze SA. Vesicular trafficking and autophagosome formation. Cell Death Differ 2009; 16: 956-965.
59. Martinet W, De Meyer GR, Andries L, Herman AG, Kockx MM. Detection of autophagy in tissue by standard immunohistochemistry: possibilities and limitations. Autophagy 2006; 2: 55-57.
60. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004; 15: 1101-1111.
61. Klionsky DJ, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4: 151-175.
62. Tanida I. Autophagy basics. Microbiol Immunol 2011; 55: 1-11.
63. Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005; 171: 603-614.
64. Komatsu M, Wang QJ, Holstein GR, Friedrich VL Jr, Iwata J, Kominami E, Chait BT, Tanaka K, Yue Z. Essential role for autophagy protein Atg7 in the maintenance of axonal homeostasis and the prevention of axonal degeneration. Proc Natl Acad Sci USA 2007; 104: 14489-14494.
65. Wang QJ, Ding Y, Kohtz DS, Mizushima N, Cristea IM, Rout MP, Chait BT, Zhong Y, Heintz N, Yue Z. Induction of autophagy in axonal dystrophy and degeneration. J Neurosci 2006; 26: 8057-8068.
66. Debnath J, Baehrecke EH, Kroemer G. Does autophagy contribute to cell death? Autophagy 2005; 1: 66-74.
67. Gump JM, Thorburn A. Autophagy and apoptosis: what is the connection? Trends Cell Biol 2011; 21: 387-392.
68. Kroemer G, Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol 2008; 12: 1004-1010.
69. Yu L, Wan F, Dutta S, Welsh S, Liu Z, Freundt E, Baehrecke EH, Lenardo M. Autophagic programmed cell death by selective catalase degradation. Proc Natl Acad Sci USA 2006; 103: 4952-4957.
70. Clarke PGH. Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 1990; 181: 195-213.
71. Galluzzi L, Vanden Berghe T, Vanlangenakker N, Buettner S, Eisenberg T, Vandenabeele P, Madeo F, Kroemer G. Programmed necrosis from molecules to health and disease. Int Rev Cell Mol Biol 2011; 289: 1-35.
72. Overholtzer M, Mailleux AA, Mouneimne G, Normand G, Schnitt SJ, King RW, Cibas ES, Brugge JS. A nonapoptotic cell death process, entosis, that occurs by cell-in-cell invasion. Cell 2007; 131: 966-979.
73. Jeanneteau F, Garabedian MJ, Chao MV. Activation of Trk neurotrophin receptors by glucocorticoids provides a neuroprotective effect. Proc Natl Acad Sci USA 2008; 105: 4862-4867.
74. Rogatsky I, Wang JC, Derynck MK, Nonaka DF, Khodabakhsh DB, Haqq CM, Darimont BD, Garabedian MJ, Yamamoto KR. Target-specific utilization of transcriptional regulatory surfaces by the glucocorticoid receptor. Proc Natl Acad Sci USA 2003; 100: 13845-13850.
75. Hamer DW, Santer RM. Anatomy and blood supply of the coeliac-superior mesenteric ganglion complex of the rat. Anat Embryol 1981; 162: 353-362.