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Spontaneous neurite outgrowth and vasoactive intestinal peptide-Iike immunoreactivity of cultures of human paraganglioma cells from the glomus jugulare

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Summary

The chief cells of paraganglionic tissues have morphological and functional similarities to adrenal chromaffin cells, and both cell types are derived from the neural crest. In the present investigation cells from two glomus jugulare paragangliomas were studied in culture. Approximately 50% of the cells from one tumor, and 7% from the other spontaneously formed neurite-like processes. Numerous granular and agranular synaptic-like vesicles also appeared in the process-forming cells. In contrast to findings with normal and neoplastic adrenal chromaffin cells, addition of nerve growth factor (NGF) to the culture medium had no major effects on proportion of cells with processes. Dexamethasone caused only a small decrease in process length. Culturing of the tumors also appeared to promote production of material with VIP-like immunoreactivity. It is concluded that the phenotype of paraganglioma as well as pheochromocytoma cells may be altered in vitro. Responsiveness to specific factors such as NGF or steroids, however, may vary for related tumor cell types in different anatomic locations.

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References

  • Böck P (1980a) Adenine nucleotides in the carotid body. Cell Tissue Res 206:279–290

    Google Scholar 

  • Böck P (1980b) Noradrenaline and acidic proteins in four types of cat carotid body chief cells. Arch Histol Jpn 43:23–34

    Google Scholar 

  • Bornstein MB (1958) Reconstituted rat-tail collagen used as a substrate for tissue culture on coverslips on Maximow slides and roller tubes. Lab Invest 7:134–140

    Google Scholar 

  • Capella D, Solcia E (1971) Optical and electron microscopic study of cytoplasmic granules in human carotid body, carotid body tumors, and glomus jugulare tumors. Virchows Arch (Cell Pathol) 7:37–53

    Google Scholar 

  • Coupland RE (1971) Observations on the form and size distribution of chromaffin granules and in the identity of adrenaline and noradrenaline-storing chromaffin cells in vertebrates and man. Mem Soc Endocrinol 19:611

    Google Scholar 

  • Desbuquois B (1974) The interaction of vasoactive intestinal peptide and secretin with liver cell membranes. Eur J Biochem 46:439–450

    Google Scholar 

  • Droz B, Rambourg A, Koenig HL (1975) The smooth endoplasmic reticulum: Structure and role in the renewal of axonal membrane and synaptic vesicles by fast axonal transport. Brain Res 93:1–13

    Google Scholar 

  • Glenner GG, Grimley PM (1974) Tumors of the extra-adrenal paraganglion system. Atlas of tumor pathology, Series 2, Fascicle 9, Armed Forces Institute of Pathology, Washington, DC, p 61

    Google Scholar 

  • Gonzales-Angulo A, Feria-Velasco A, Corvera J, Elias EY (1968) Ultrastructure of the glomus jugulare tumor. Arch Otolaryngol 87:30–39

    Google Scholar 

  • Greene LA (1977) A quantitative bioassay for nerve growth factor (NGF) activity employing a clonal pheochromocytoma cell line. Brain Res 133:350–353

    Google Scholar 

  • Greene LA, Tischler AS (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci (USA) 73:2424–2428

    Google Scholar 

  • Harper GP, Pearce FL, Vernon CA (1976) Production of nerve growth factor in the mouse adrenal medulla. Nature 261:251–253

    Google Scholar 

  • Kjaergaard J (1973) Anatomy of the Carotid Glomus and Carotid Glomus-like Bodies (Non-chromaffin Paraganglia). With Electron Microscopy and Comparison of Human Foetal Carotid, Aorticopulmonary, Subclavian, Tympanojugular, and Vagal Glomera. Translated from the Danish by LaCour, A. Copenhagen: F.A.D.L.'s Forlag, p 279

    Google Scholar 

  • Kobayashi S, Serizawa Y (1980) Adrenal chromaffin cells in the stressed mouse. In: Eränkö O, Soinilla S, Paivarinta H (eds) Histochemistry and Cell Biology of Autonomic Neurons, SIF Cells and Paraneurons. Raven Press, NY, p 195

    Google Scholar 

  • Linnoila RI, DiAugustine RP, Hervonen A, Miller RJ (1980) Distribution of [Met3] and [Leu5]-enkephalin-, VIP-, and substance P-like immunoreactivity in human adrenal glands. Neurosci 5:2247–2259

    Google Scholar 

  • Livett BG, Dean DM, Bray GM (1978) Growth characteristics of isolated adrenal medullary cells in culture. Soc Neurosci Abstr 4:592

    Google Scholar 

  • Luckenbill-Edds L, Van Horn C, Greene LA (1979) Fine structure of initial outgrowth of processes induced in a pheochromocytoma cell line (PC 12) by nerve growth factor. J Neurocytol 8:493–511

    Google Scholar 

  • Lundberg JM, Hökfelt T, Fahrenkrug JF, Nilsson G, Terenius L (1979) Peptides in the rat carotid body (glomus caroticum): VIP-, enkephalin- and substance P-like immunoreactivity. Acta Physiol Scand 107:279–283

    Google Scholar 

  • Mendelsohn G, Eggleston JC, Olson JL, Said SI, Baylin SB (1979) Vasoactive intestinal peptide and its relationship to ganglion cell differentiation in neuroblastic tumors. Lab Invest 41:144–149

    Google Scholar 

  • Pais SO (1978) Angiographic demonstration of a vasoactive intestinal polypeptide secreting pheochromocytoma in a patient with WDHA syndrome. Am J Roentgenol 130:172–174

    Google Scholar 

  • Pandian MR, Horvat A, Said SI (1981) Radioimmunoassay of VIP in blood and tissue. In: Said SI (ed) Vasoactive intestinal peptide. Raven Press, New York (in Press)

    Google Scholar 

  • Pearse AGE (1977) The diffuse neuroendocrine system and the APUD concept: Related “endocrine” peptides in brain, intestine, pituitary, placenta and anuran cutaneous glands. Med Biol 55:115–125

    Google Scholar 

  • Pintar JE (1978) Distribution and synthesis of glycosaminoglycans during quail neural crest morphogenesis. Dev Biol 67:444–464

    Google Scholar 

  • Pryse-Davies J, Dawson IMP, Westbury G (1964) Some morphologic, histochemical and chemical observations on chemodectomas and the normal carotid body, including a study of the chromaffin reaction and possible ganglion cell elements. Cancer 17:185–202

    Google Scholar 

  • Said SI, Faloona GR (1975) Elevated plasma and tissue levels of vasoactive intestinal polypeptide in the watery diarrhea syndrome due to pancreatic, bronchogenic and other tumors. N Engl J Med 293:155–160

    Google Scholar 

  • Sternberger LA (1979) Immunocytochemistry. Second Ed, John Wiley and Sons, New York, NY

    Google Scholar 

  • Sumerson LF (1970) Glomus jugulare tumors: A comprehensive study with report of case. J Am Osteopathol Assoc 70:146–161

    Google Scholar 

  • Tischler AS, Greene LA (1975) Nerve growth factor-induced process formation by cultured rat pheochromocytoma cells. Nature 258:341–342

    Google Scholar 

  • Tischler AS, Greene LA (1978) Morphologic and cytochemical properties of a clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Lab Invest 39:77–89

    Google Scholar 

  • Tischler AS, Dichter MA, Biales B, DeLellis RA, Wolfe HJ (1976) Neural properties of cultured human endocrine tumor cells of proposed neural crest origin. Science 192:902–904

    Google Scholar 

  • Tischler AS, DeLellis RA, Biales B, Nunnemacher G, Carraba V, Wolfe HJ (1980) Nerve growth factor-induced neurite outgrowth from normal human chromaffin cells. Lab Invest 43:399–409

    Google Scholar 

  • Unsicker K, Chamley JH (1977) Growth characteristics of postnatal rat adrenal medulla in culture. Cell Tissue Res 177:247–268

    Google Scholar 

  • Unsicker K, Krisch B, Otten U, Thoenen H (1978) Nerve growth factor-induced fiber outgrowth from isolated rat adrenal chromaffin cells: impairment by glucocorticoids. Proc Natl Acad Sci (USA) 75:3498

    Google Scholar 

  • Unsicker K, Griesser GH, Lindmar R, Löffelholz K, Wolfe U (1980) Establishement, characterization and fibre outgrowth of isolated bovine adrenal medullary cells in long-term cultures. Neurosci 5:1445–1460

    Google Scholar 

  • Varon S, Raiborn C (1972) Dissociation, fractionation and culture of chick embryo sympathetic ganglionic cells. J Neurocytol 1:211–221

    Google Scholar 

  • Wharton J, Polak JM, Pearse AGE, McGregor GP, Bryant MG, Bloom SR, Emson PC, Bisgard GE, Will JA (1980) Enkephalin-, VIP- and substance P-like immunoreactivity in the carotid body. Nature 284:269–271

    Google Scholar 

  • Young DM, Oger J, Blanchard MH, Asdourian H, Arnason BGW (1975) Secretion of a nerve growth factor by primary chick fibroblast cultures. Science 187:361–363

    Google Scholar 

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Tischler, A.S., Lee, A.K., Nunnemacher, G. et al. Spontaneous neurite outgrowth and vasoactive intestinal peptide-Iike immunoreactivity of cultures of human paraganglioma cells from the glomus jugulare. Cell Tissue Res. 219, 543–555 (1981). https://doi.org/10.1007/BF00209993

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