Abstract
Chromaffin cells probably are the most intensively studied of the neural crest derivates. They are closely related to the nervous system, share with neurons some fundamental mechanisms and thus were the ideal model to study the basic mechanisms of neurobiology for many years. The lessons we have learned from chromaffin cell biology as a peripheral model for the brain and brain diseases pertain more than ever to the cutting edge research in neurobiology. Here, we highlight how studying this cell model can help unravel the basic mechanisms of cell renewal and regeneration both in the central nervous system (CNS) and neuroendocrine tissue and also can help in designing new strategies for regenerative therapies of the CNS.
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References
Helle KB, Reed RK, Ehrhart M, Aunis D, Hogue AR . Chromogranin A: osmotically active fragments and their susceptibility to proteolysis during lysis of the bovine chromaffin granules. Acta Physiol Scand 1990; 138: 565–574.
Thiele C, Hannah MJ, Fahrenholz F, Huttner WB . Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat Cell Biol 2000; 2: 42–49.
Winkler H . The adrenal chromaffin granule: a model for large dense core vesicles of endocrine and nervous tissue. J Anat 1993; 183 (Part 2): 237–252.
DĂaz-Vera J, Morales YG, Hernandez-Fernaud JR, Camacho M, Montesinos MS, Calegari F et al. Chromogranin B gene ablation reduces the catecholamine cargo and decelerates exocytosis in chromaffin secretory vesicles. J Neurosci 2010; 30: 950–957.
Stevens DR, Schirra C, Becherer U, Rettig J . Vesicle pools: lessons from adrenal chromaffin cells. Front Synaptic Neurosci 2011; 3: 2.
Negri L, Melchiorri P, Höckfelt T, Nisticò G . In Memory of Vittorio Erspamer. Exorma Pub. Co.: Rome, 2009.
Greene LA, Tischler AS . Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA 1976; 73: 2424–2428.
Miele E, Rubin RP . Secretion of adrenaline and noradrenaline from the perfused cat adrenal gland. Br J Pharmacol 1968; 34: 691P.
Miele E . Effect of metoclopramide and structurally related agents on the catecholamine secretion of the perfused cat adrenal medulla. Farmaco Prat 1970; 25: 383–392.
Drucker-Colin R, Verdugo-Diaz L . Cell transplantation for Parkinson's disease: present status. Cell Mol Neurobiol 2004; 24: 301–316.
Fernandez-Espejo E, Armengol JA, Flores JA, Galan-Rodriguez B, Ramiro S . Cells of the sympathoadrenal lineage: biological properties as donor tissue for cell-replacement therapies for Parkinson's disease. Brain Res Brain Res Rev 2005; 49: 343–354.
Quinn NP . The clinical application of cell grafting techniques in patients with Parkinson's disease. Prog Brain Res 1990; 82: 619–625.
Vrezas I, Willenberg HS, Mansmann G, Hiroi N, Fritzen R, Bornstein SR . Ectopic adrenocorticotropin (ACTH) and corticotropin-releasing hormone (CRH) production in the adrenal gland: basic and clinical aspects. Microsc Res Tech 2003; 61: 308–314.
Bornstein SR, Schuppenies A, Wong ML, Licinio J . Approaching the shared biology of obesity and depression: the stress axis as the locus of gene-environment interactions. Mol Psychiatry 2006; 11: 892–902.
Haase M, Willenberg HS, Bornstein SR . Update on the corticomedullary interaction in the adrenal gland. Endocr Dev 2011; 20: 28–37.
Bornstein SR, Tian H, Haidan A, Bottner A, Hiroi N, Eisenhofer G et al. Deletion of tyrosine hydroxylase gene reveals functional interdependence of adrenocortical and chromaffin cell system in vivo. Proc Natl Acad Sci USA 2000; 97: 14742–14747.
Ehrhart-Bornstein M, Hinson JP, Bornstein SR, Scherbaum WA, Vinson GP . Intraadrenal interactions in the regulation of adrenocortical steroidogenesis. Endocr Rev 1998; 19: 101–143.
Yao M, Schulkin J, Denver RJ . Evolutionarily conserved glucocorticoid regulation of corticotropin-releasing factor expression. Endocrinology 2008; 149: 2352–2360.
Ziegler CG, Langbein H, Krug AW, Ludwig B, Eisenhofer G, Ehrhart-Bornstein M et al. Direct effect of dehydroepiandrosterone sulfate (DHEAS) on PC-12 cell differentiation processes. Mol Cell Endocrinol 2011; 336: 149–155.
Miele E, Rosati P, Gargiulo G, Anania V . Effect of adrenal steroidogenesis inhibition by aminoglutethimide on the catecholamine content and on the adrenaline- and noradrenaline-storing cells pattern of the rat adrenal medulla. Arch Int Pharmacodyn Ther 1972; 196 (Suppl 196): 309.
Miele E . Effects of steroidogenesis inhibition or stimulation on the catecholamine content and on responsiveness of the cat adrenal medulla. Pharmacol Res Comm 1969; 1: 369–379.
Lu L, Shimizu T, Nakamura K, Yokotani K . Brain neuronal/inducible nitric oxide synthases and cyclooxygenase-1 are involved in the bombesin-induced activation of central adrenomedullary outflow in rats. Eur J Pharmacol 2008; 590: 177–184.
Levi-Montalcini R, Calissano P . The nerve-growth factor. Sci Am 1979; 240: 68–77.
Bornstein SR, Yoshida-Hiroi M, Sotiriou S, Levine M, Hartwig HG, Nussbaum RL et al. Impaired adrenal catecholamine system function in mice with deficiency of the ascorbic acid transporter (SVCT2). FASEB J 2003; 17: 1928–1930.
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.
Aloe L, Levi-Montalcini R . Nerve growth factor-induced transformation of immature chromaffin cells in vivo into sympathetic neurons: effect of antiserum to nerve growth factor. Proc Natl Acad Sci USA 1979; 76: 1246–1250.
Krieglstein K, Unsicker K . Proteins from chromaffin granules promote survival of dorsal root ganglionic neurons: comparison with neurotrophins. Brain Res Dev Brain Res 1996; 93: 10–17.
Matrone C, Di LA, Meli G, D'Aguanno S, Severini C, Ciotti MT et al. Activation of the amyloidogenic route by NGF deprivation induces apoptotic death in PC12 cells. J Alzheimers Dis 2008; 13: 81–96.
Matrone C, Marolda R, Ciafre S, Ciotti MT, Mercanti D, Calissano P . Tyrosine kinase nerve growth factor receptor switches from prosurvival to proapoptotic activity via Abeta-mediated phosphorylation. Proc Natl Acad Sci USA 2009; 106: 11358–11363.
Shimoke K, Sasaya H, Ikeuchi T . Analysis of the role of nerve growth factor in promoting cell survival during endoplasmic reticulum stress in PC12 cells. Methods Enzymol 2011; 490: 53–70.
Ravni A, Bourgault S, Lebon A, Chan P, Galas L, Fournier A et al. The neurotrophic effects of PACAP in PC12 cells: control by multiple transduction pathways. J Neurochem 2006; 98: 321–329.
Suk K, Park JH, Lee WH . Neuropeptide PACAP inhibits hypoxic activation of brain microglia: a protective mechanism against microglial neurotoxicity in ischemia. Brain Res 2004; 1026: 151–156.
Sun L, Guo C, Liu D, Zhao Y, Zhang Y, Song Z et al. Protective effects of bone morphogenetic protein 7 against amyloid-beta induced neurotoxicity in PC12 cells. Neuroscience 2011; 184: 151–163.
Sun ZP, Gong L, Huang SH, Geng Z, Cheng L, Chen ZY . Intracellular trafficking and secretion of cerebral dopamine neurotrophic factor in neurosecretory cells. J Neurochem 2011; 117: 121–132.
Licinio J, Dong C, Wong ML . Novel sequence variations in the brain-derived neurotrophic factor gene and association with major depression and antidepressant treatment response. Arch Gen Psychiatry 2009; 66: 488–497.
Tan Y, Duan J, Li Y, Cai W . Effects of citalopram on serum deprivation induced PC12 cell apoptosis and BDNF expression. Pharmazie 2010; 65: 845–848.
Ehrhart-Bornstein M, Vukicevic V, Chung KF, Ahmad M, Bornstein SR . Chromaffin progenitor cells from the adrenal medulla. Cell Mol Neurobiol 2010; 30: 1417–1423.
Chung KF, Sicard F, Vukicevic V, Hermann A, Storch A, Huttner WB et al. Isolation of neural crest derived chromaffin progenitors from adult adrenal medulla. Stem Cells 2009; 27: 2602–2613.
Ehrhart-Bornstein M, Chung KF, Vukicevic V, Bornstein SR . Is there a role for chromaffin progenitor cells in neurodegenerative diseases? Mol Psychiatry 2009; 14: 1–4.
Perez-Alvarez A, Hernandez-Vivanco A, Albillos A . Past, present and future of human chromaffin cells: role in physiology and therapeutics. Cell Mol Neurobiol 2010; 30: 1407–1415.
Lindvall O, Kokaia Z . Prospects of stem cell therapy for replacing dopamine neurons in Parkinson's disease. Trends Pharmacol Sci 2009; 30: 260–267.
Louvi A, Artavanis-Tsakonas S . Notch signalling in vertebrate neural development. Nat Rev Neurosci 2006; 7: 93–102.
Yoon K, Gaiano N . Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat Neurosci 2005; 8: 709–715.
Vialli M, Erspamer V . Ricerche sul secreto delle cellule enterocromaffini. Boll Soc Med Chir 1937; 27: 81–99.
Erspamer V, Asero B . Identification of enteramine, the specific hormone of the enterochromaffin cell system, as 5-hydroxytryptamine. Nature 1952; 169: 800–801.
Amin AH, Crawford TB, Gaddum JH . The distribution of substance P and 5-hydroxytryptamine in the central nervous system of the dog. J Physiol 1954; 126: 596–618.
Tischler AS . Chromaffin cells as models of endocrine cells and neurons. Ann N Y Acad Sci 2002; 971: 366–370.
Androutsellis-Theotokis A, Rueger MA, Park DM, Mkhikian H, Korb E, Poser SW et al. Targeting neural precursors in the adult brain rescues injured dopamine neurons. Proc Natl Acad Sci USA 2009; 106: 13570–13575.
Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW et al. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 2006; 442: 823–826.
Androutsellis-Theotokis A, Rueger MA, Mkhikian H, Korb E, McKay RD . Signaling pathways controlling neural stem cells slow progressive brain disease. Cold Spring Harb Symp Quant Biol 2008; 73: 403–410.
Androutsellis-Theotokis A, Walbridge S, Park DM, Lonser RR, McKay RD . Cholera toxin regulates a signaling pathway critical for the expansion of neural stem cell cultures from the fetal and adult rodent brains. PLoS One 2010; 5: e10841.
Androutsellis-Theotokis A, Rueger MA, Park DM, Boyd JD, Padmanabhan R, Campanati L et al. Angiogenic factors stimulate growth of adult neural stem cells. PLoS One 2010; 5: e9414.
Kohn A . Über die Nebenniere. Prag med Wochenschrift 1898; 23: 193–195.
Kohn A . Das chromaffine Gewebe. Ergebn Anat Entwickl-Gesch 1902; 12: 253–348.
Kohn A . Die Paraganglien. Arch Mikr Anat 1903; 62: 263–365.
Acknowledgements
This work was supported by grants of the Deutsche Forschungsgemeinschaft: KFO 252/1 (SRB, MEB, AAT, GE), SFB 655 (MEB, SRB) and the Center for Regenerative Therapies Dresden Cluster of Excellence to (SRB, MEB).
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Bornstein, S., Ehrhart-Bornstein, M., Androutsellis-Theotokis, A. et al. Chromaffin cells: the peripheral brain. Mol Psychiatry 17, 354–358 (2012). https://doi.org/10.1038/mp.2011.176
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DOI: https://doi.org/10.1038/mp.2011.176
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