Evolution of the diffuse neuroendocrine system - Clear cells and cloudy origins

Neuroendocrinology

Volumn 84, Issue 2, 2007, Pages 69-82

  Modlin, Irvin M ^a   Champaneria, Manish C ^a   Bornschein, Jan ^a   Kidd, Mark ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

'APUD'; Cajal; Carcinoid; Clear cells; Feyrter; Neuroendocrine; Pearse

Indexed keywords

AUTONOMIC NERVOUS SYSTEM; CELL FUNCTION; CELL LINEAGE; CHROMAFFIN CELL; ENDOCRINE CELL; ENDOCRINE GLAND; HOMEOSTASIS; HORMONAL REGULATION; HORMONE ACTION; HUMAN; INTERSTITIAL CELL OF CAJAL; MYENTERIC PLEXUS; NEUROENDOCRINOLOGY; NEUROTRANSMISSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SCHWANN CELL; SMOOTH MUSCLE FIBER; STOMACH GLAND;

ANIMALS; APUD CELLS; CELL COMMUNICATION; ENTEROENDOCRINE CELLS; GASTROENTEROLOGY; GASTROINTESTINAL HORMONES; HISTORY, 16TH CENTURY; HISTORY, 17TH CENTURY; HISTORY, 18TH CENTURY; HISTORY, 19TH CENTURY; HISTORY, 20TH CENTURY; HISTORY, ANCIENT; HORMONES; HUMANS; NEUROENDOCRINOLOGY; NEUROSECRETORY SYSTEMS; PORTRAITS;

EID: 33846444742     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000096997     Document Type: Review

References (117)

1. Mettler CC: History of Medicine. Philadelphia, Blakiston, 1947.
2. Needham J: Proto-Endocrinology in Medieval China. Cambridge, Cambridge University Press, 1966.
3. Himes NE: A Medical History of Contraception. New York, Gamut Press, 1936.
4. Harris GW: Humours and hormones. J Endocrinol 1972;53:2-23.
5. Vesalius A: De humani corporis fabrica librii septem. Basel, Oporinus, 1543.
6. Wharton T: Adenographia sive glandularum totius corporis description. London, Coll. Lond. Socii Amstelaedami, 1659.
7. Modlin IM, Kidd M: The Paradox of the Pancreas: from Wirsung to Whipple. Hanover, Politzki Print Productions, 2003.
8. Haller AV: Elementa physiologiae corporis humani. Lausanne, 1757-1766.
9. Sharpey-Schafer E: Endocrine physiology. Irish J Med Sci 1931;69:483-505.
10. Schleiden MJ: Beiträge zur Phytogenesis. Arch Anat Physiol 1838, pp 137-176.
11. Hughes A: A History of Cytology. London, Abelard-Schuman, 1959.
12. Schwann T: Ueber das Wesen des Verdauungsprocesses. Arch Anat Physiol 1836: 90-138.
13. Schwann T: Mikroskopische Untersuchungen über Übereinstimmung in der Struktur und dem Wachsthum der Thiere und Pflanzen. Berlin, Verlag der Sanderschen Buchhandlung, 1839.
14. Virchow R: Die Cellularpathologie, ed 4. Berlin, Hirschwald, 1871.
15. Bernard C: Sur une nouvelle fonction du foie chez l'homme et les animaux. CR Acad Sci 1850;31:571-574.
16. Hunter J: Observations on Certain Parts of the Animal Oeconomy. London, 1786.
17. Addison T: On the Constitution and Local Effects of Diseases of the Supra Renal Capsules. London, Samuel Highley, 1855.
18. Brown-Séquard CE: Recherches expérimentales sur la physiologie et la pathologie des capsules surrénales. CR Acad Sci 1856;43:422-425.
19. Oliver G, Schaefer EA: On the physiological action of extract of the suprarenal capsules. J Physiol 1894;17:i-v.
20. Kocher T: Concerning pathological manifestations in low-grade thyroid diseases. Nobel-Lecture, 1909.
21. Heidenhain RP: Untersuchungen über den Bau der Labdrüsen. Arch Mikr Anat 1870;6:368-406.
22. Langerhans P: Beiträge zur mikroskopi schen Anatomie der Bauchspeicheldrüse. Berlin, 1869.
23. Laguesse GE: Sur la formation des Ilots de Langerhans dans le pancréas. CR Soc Biol 1893;5:819-820.
24. Kulchitsky N: Zur Frage über den Bau des Darmkanals. Arch Mikr Anat 1897;49:7-35.
25. Pavlov IP: Die Innervation des Pankreas. Klin Wochenzeitung 1888;32:667-675.
26. Pavlov IP: Lektsii o rabote glavnykh pischchevaritel'nykh zhelez (The work of the digestive glands). St. Petersburg, Piroda, 1897.
27. Bayliss WM, Starling EH: The mechanism of pancreatic secretion. J Physiol 1902;28:325-353.
28. Martin C: Ernest Henry Starling (obituary). Br Med J 1927;i:900-906.
29. Starling EH: The Croonian Lectures on the chemical correlation of the functions of the body. Lancet 1905;166:339-341.
30. Garrison FH: History of Medicine, ed 4, Philadelphia, Saunders, 1929.
31. David K: Über krystallinisches männliches Hormon aus Hoden (Testosteron) wirksamer als aus Harn oder aus Cholesterin bereitetes Androsteron. Z Physiol Chem 1935;233:281.
32. Collip JB: The extraction of a parathyroid hormone which will prevent or control parathyroid tetany and which regulates the level of blood calcium. J Biol Chem 1925;63:395-438.
33. Cushing H: The basophil adenomas of the pituitary body and their clinical manifestations (pituitary basophilism). Bull Johns Hopkins Hosp 1932;50:137-195.
34. Kendall EC: A method for the decomposition of the proteins of the thyroid, with a description of certain constituents. J Biol Chem 1915;20:501-509.
35. Banting FG: The internal secretion of the pancreas. J Lab Clin Med 1922;7:253.
36. Medvei VC: The History of Clinical Endocrinology, ed 2. New York, Parthenon, 1993.
37. Ramón y Cajal S: Nuevas aplicationes del método de coloración de Golgi. Gaceta Médica Catalana 1889;12:613-616.
38. Ramón y Cajal S: Sur les ganglions et plexus nerveux de l'intestin. CR Soc Biol 1893;45:217-223.
39. The Nobel Prize Winners - Physiology or Medicine. Pasadena, Salem Press, 1991. 40 Golgi C: On the structure of the brain grey matter. Gaz Med Ital, 1873.
40. Ramón y Cajal S: Histologie du système nerveux de l'homme et des vertébrés. Grand sympathique. Paris, Maloine, 1911, vol 2, pp 891-942.
41. Keith A: An account of six specimens of the great bowel removed by operation: with some observations on the motor mechanism of the colon. Br J Surg 1914;2:576-599.
42. Keith A: A new theory of the causation of enterostasis. Lancet 1915;ii:371-375.
43. Thuneberg L: One hundred years of interstitial cells of Cajal. Microsc Res Tech 1999;47:223-238.
44. Lawrentjew BI: Über die nervöse Natur und das Vorkommen der sogenannten interstitiellen Zellen (Cajal, Dogiel) in der glatten Muskulatur. Proc Kon Acad Wetensch 1925;28:977-983.
45. Feyrter F: Standardization of silver impregnation of neural and non-neural tissues. Virchows Arch 1951;320:551-563.
46. Meyling HA: Structure and significance of the peripheral extension of the autonomic nervous system. J Comp Neurol 1953;99:495-543.
47. Jabonero V: Plexiform synapse of distance and significance of so-called intercalated cells. Acta Neuroveg (Wien) 1959;19:276-302.
48. Taxi J: Contribution á l'étude des connexions des neurones moteurs du système nerveux autonome. Ann Sci Nat Zool 1965;7:413-674.
49. Taxi J: Sur la structure des travées du plexus d'Auerbach: Confrontation des données fournies par le microscope ordinaire et par le microscope électronique. Ann Sci Nat Zool 1959;1:571-593.
50. Taxi J: Cellules de Schwann et 'cellules interstitielles de Cajal' au niveau des plexus nerveuz de la musculeuse intestinale du cobaye: retour aux définitions. Arch Anat Microsc 1952;41:281-304.
51. Tinel J: Le Systéme Nerveux Végétatif. Paris, Libr l'Acad Méd, 1937.
52. Imaizumi M, Hama K: An electron microscopic study on the interstitial cells of the gizzard in the love-bird (Uroloncha domestica). Z Zellforsch Mikrosk Anat 1969;97:351-357.
53. Yamamoto M: Electron microscopic studies on the innervation of the smooth muscle and the interstitial cell of Cajal in the small intestine of the mouse and bat. Arch Histol Jpn 1977;40:171-201.
54. Daniel EE: Nerves and motor activity of the gut; in Brooks FPE (ed): Nerves and the Gut. New York, Slack, 1977, pp 154-196.
55. Ambache N: The electrical activity of isolated mammalian intestines. J Physiol 1947;106:139-153.
56. Thuneberg L: Interstitial cells of Cajal: intestinal pacemaker cells? Adv Anat Embryol Cell Biol 1982;71:1-130.
57. Stach W: The extreme enteric plexus of the large intestine and its relation to the interstitial cells (Cajal). Z Mikrosk Anat Forsch 1972;85:245-272.
58. Barajas-Lopez C, Berezin I, Daniel EE, Huizinga JD: Pacemaker activity recorded in interstitial cells of Cajal of the gastrointestinal tract. Am J Physiol 1989;257:C830-C835.
59. Lee JC, Thuneberg L, Berezin I, Huizinga JD: Generation of slow waves in membrane potential is an intrinsic property of interstitial cells of Cajal. Am J Physiol 1999;277:G409-G423.
60. Faussone-Pellegrini MS: Histogenesis, structure and relationships of interstitial cells of Cajal (ICC): from morphology to functional interpretation. Eur J Morphol 1992;30:137-148.
61. Maeda H, Yamagata A, Nishikawa S, Yoshinaga K, Kobayashi S, Nishi K, Nishikawa S: Requirement of c-kit for development of intestinal pacemaker system. Development 1992;116:369-375.
62. Ward SM, Burns AJ, Torihashi S, Sanders KM: Mutation of the proto-oncogene c-kit blocks development of interstitial cells and electrical rhythmicity in murine intestine. J Physiol 1994;480:91-97.
63. Huizinga JD, Thuneberg L, Kluppel M, Malysz J, Mikkelsen HB, Bernstein A: W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature 1995;373:347-349.
64. Romert P, Mikkelsen HB: c-kit immunoreactive interstitial cells of Cajal in the human small and large intestine. Histochem Cell Biol 1998;109:195-202.
65. Lecoin L, Gabella G, Le Douarin N: Origin of the c-kit-positive interstitial cells in the avian bowel. Development 1996;122:725-733.
66. Kluppel M, Huizinga JD, Malysz J, Bernstein A: Developmental origin and Kit-dependent development of the interstitial cells of Cajal in the mammalian small intestine. Dev Dyn 1998;211:60-71.
67. Torihashi S, Ward S, Sanders K: Development of c-Kit-positive cells and the onset of electrical rhythmicity in murine small intestine. Gastroenterology 1997;112:144-155.
68. Torihashi S, Nishi K, Tokutomi Y, Nishi T, Ward S, Sanders K: Blockade of kit signaling induces transdifferentiation of interstitial cells of Cajal to a smooth muscle phenotype. Gastroenterology 1999;117:140-148.
69. Burns AJ, Lomax AE, Torihashi S, Sanders KM, Ward SM: Interstitial cells of Cajal mediate inhibitory neurotransmission in the stomach. Proc Natl Acad Sci USA 1996;93:12008-12013.
70. Ward SM, Morris G, Reese L, Wang XY, Sanders KM: Interstitial cells of Cajal mediate enteric inhibitory neurotransmission in the lower esophageal and pyloric sphincters. Gastroenterology 1998;115:314-329.
71. Schiefferdecker P: Über die Neuronen und die innere Sekretion. Sitzgsber Niedderrhein Ges Naturheilkd 1905, pp 46-54.
72. Tigerstedt RA: Niere und Kreislauf. Scand Arch Physiol 1898;8:223-271.
73. Cannon WB: The emergency function of the adrenal medulla in pain and the major emotions. Am J Physiol 1914;33:356-372.
74. Elliott TR: The innervation of the bladder and urethra. J Physiol 1907;35:367-445.
75. Loewi O: Über humorale Übertragbarkeit der Herznervenwirkung. Pflügers Arch ges Physiol 1921;189:239-242.
76. Nicolas A: Recherches sur l'épithélium de l'intestine grele. Int Mschr Anat Physiol 1891;8:1-8.
77. Schmidt JE: Beiträge zur normalen und pathologischen Histologie einiger Zellarten der Schleimhaut des menschlichen Darm-Kanals. Arch Mikrosk Anat 1905;66:12-40.
78. Ciaccio C: Ricerche istologiche e citologiche sul timo degli Uccelli. Anat Anz 1906;29:597-600.
79. Ciaccio C: Sur une nouvelle espéce cellulaire dans les glandes de Lieberkühn. CR Soc Biol Paris 1906;60:76-77.
80. Masson P: La glande endocrine de l'intestin chez l'homme. CR Acad Sci 1914;158:59-61.
81. Gosset A, Masson P: Tumeurs endocrines de l'appendice. Presse Med 1914;25:237-240.
82. Masson P: Carcinoids (argentaffin-cell tumors) and nerve hyperplasia of the appendicular mucosa. Am J Path 1928;4:181-212.
83. Erös G: Über die argentaffinen Zellen der Schleimhaut des Magen-Darmtraktes. Frankf Z Pathol 1928;36:402.
84. Erös G: Über die Bedeutung der argentaffinen Zellen. Frankf Z Pathol 1931;40:155.
85. Erös G: Eine neue Darstellungsmethode der sogenannten gelben argentaffinen Zellen des Magen-Darmtraktes. Zbl Path 1932;54:385.
86. Kahlau G: Versuch zur Beeinflussung der gelben Zellen des Darmes durch Hormone. Z Exper Med 1931;80:190.
87. Feyrter F: Über diffuse endocrine epitheliale Organe. Leipzig, Barth, 1938.
88. Feyrter F: Karzinoid und Karzinom. Ergebn Allg Pathol Anat 1934;29:305-489.
89. Hakanson R, Sundler F: APUD cells in rat oxyntic mucosa. Gastroenterology 1979;77:800-803.
90. Capella C, Polak JM, Timson CM, Frigerio B, Solcia E: Gastric carcinoids of argyrophil ECL cells. Ultrastruct Pathol 1980;1:411-418.
91. Modlin IM, Kidd M, Pfragner R, Eick GN, Champaneria MC: The functional characterization of normal and neoplastic human enterochromaffin cells. J Clin Endocrinol Metab 2006;91:2340-2348.
92. Modlin IM, Kidd M, Latich I, Zikusoka MN, Shapiro MD: Current status of gastrointestinal carcinoids. Gastroenterology 2005;128:1717-1751.
93. Masson P: Appendicite neurogene et carcinoides. Ann Anat Path 1924;1:20.
94. Sunder-Plassmann P: Über neuro-hormonale Zellen des Vagussystem in der Schilddrüse. Dtsch Z Chir 1939;252:210-223.
95. Altmann HW: Die parafollikuläre Zelle der Schilddrüse und ihre Beziehungen zu der Gelben Zelle des Darmes. Beitr Path Anat 1940;104:419-428.
96. Pagés A: Essai sur le système des cellules claires de Feyrter. Université de Montpellier, 1955.
97. Pearse AG: The cytochemistry and ultrastructure of polypeptide hormone-producing cells of the APUD series and the embryologic, physiologic and pathologic implications of the concept. J Histochem Cytochem 1969;17:303-313.
98. Pearse AG: Common cytochemical and ultrastructural characteristics of cells producing polypeptide hormones (the APUD series) and their relevance to thyroid and ultimobranchial C cells and calcitonin. Proc R Soc Lond [B] 1968;170:71-80.
99. Pearse AG: The diffuse endocrine (paracine) system: Feyrter's concept and its modern history. Verh Dtsch Ges Pathol 1977;61:2-6.
100. Day R, Salzet M: The neuroendocrine phenotype, cellular plasticity, and the search for genetic switches: redefining the diffuse neuroendocrine system. Neuro Endocrinol Lett 2002;23:447-451.
101. Szijj I, Csapo Z, Laszlo FA, Kovacs K: Medullary cancer of the thyroid gland associated with hypercorticism. Cancer 1969;24:167-173.
102. Welbourn RB: Apudomas of the gut. Am J Surg 1977;133:13-22.
103. Langley K: The neuroendocrine concept today. Ann NY Acad Sci 1994;733:1-17.
104. Bishop AE, Polak JM: Cytochemical techniques for studying the diffuse neuroendocrine system. Methods Enzymol 1989;168:791-808.
105. Bishop AE, Power RF, Polak JM: Markers for neuroendocrine differentiation. Pathol Res Pract 1988;183:119-128.
106. Pearse AG, Polak JM: Neural crest origin of the endocrine polypeptide (APUD) cells of the gastrointestinal tract and pancreas. Gut 1971;12:783-788.
107. Pearse AG, Takor T: Embryology of the diffuse neuroendocrine system and its relationship to the common peptides. Fed Proc 1979;38:2288-2294.
108. Andrew A, Kramer B, Rawdon BB: The origin of gut and pancreatic neuroendocrine (APUD) cells - the last word? J Pathol 1998;186:117-118.
109. Andrew A, Kramer B, Rawdon BB: Gut and pancreatic amine precursor uptake and decarboxylation cells are not neural crest derivatives. Gastroenterology 1983;84:429-431.
110. Fontaine J, Le Douarin NM: Analysis of endoderm formation in the avian blastoderm by the use of quail-chick chimaeras. The problem of the neurectodermal origin of the cells of the APUD series. J Embryol Exp Morphol 1977;41:209-222.
111. Thompson M, Fleming KA, Evans DJ, Fundele R, Surani MA, Wright NA: Gastric endocrine cells share a clonal origin with other gut cell lineages. Development 1990;110:477-481.
112. Toni R: The neuroendocrine system: organization and homeostatic role. J Endocrinol Invest 2004;27:35-47.
113. Odell WD: Paraendocrine syndromes of cancer. Adv Intern Med 1989;34:325-351.
114. Gould VE, Linnoila RI, Memoli VA, Warren WH: Neuroendocrine components of the bronchopulmonary tract: hyperplasias, dysplasias, and neoplasms. Lab Invest 1983;49:519-537.
115. Tasiemski A, Salzet M, Benson H, Fricchione GL, Bilfinger TV, Goumon Y, Metz-Boutigue MH, Aunis D, Stefano GB: The presence of antibacterial and opioid peptides in human plasma during coronary artery bypass surgery. J Neuroimmunol 2000;109:228-235.
116. Suzuki S, Tanaka K, Nagata E, Ito D, Dembo T, Fukuuchi Y: Cerebral neurons express interleukin-6 after transient forebrain ischemia in gerbils. Neurosci Lett 1999;262:117-120.
117. Reichlin S: Neuroendocrine-immune interactions. N Engl J Med 1993;329:1246-1253.