Granins and granin-related peptides in neuroendocrine tumours

Regulatory Peptides

Volumn 165, Issue 1, 2010, Pages 12-20

  Portela Gomes, Guida M ^a   Grimelius, Lars ^b   Wilander, Erik ^b   Stridsberg, Mats ^b  

^a UNIVERSITY OF LISBON   (Portugal)

^b UPPSALA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Chromogranins; Granin derived peptides; Granins; Immunohistochemistry; Neuroendocrine differentiation; Neuroendocrine tumours; Prohormone convertases; Secretogranins

Indexed keywords

CHROMOGRANIN A; CHROMOGRANIN B; POLYPEPTIDE; PROPROTEIN CONVERTASE 1; PROPROTEIN CONVERTASE 2; PROPROTEIN CONVERTASE 5; REGULATOR PROTEIN; SECRETOGRANIN II; SECRETOGRANIN III; SECRETOGRANIN IV; SECRETOGRANIN V; SECRETOGRANIN VI; SECRETOGRANIN VII; SECRETONEURIN; SECRETORY PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CELL TYPE; DIAGNOSTIC VALUE; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NEUROENDOCRINE TUMOR; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVIEW; TISSUE DISTRIBUTION;

CHROMOGRANIN A; CHROMOGRANIN B; CHROMOGRANINS; HUMANS; NEUROENDOCRINE TUMORS; NEUROPEPTIDES; SECRETOGRANIN II;

EID: 78649844413     PISSN: 01670115     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.regpep.2010.02.011     Document Type: Review

References (158)

1. Volante M., Rindi G., Papotti M. The grey zone between pure (neuro)endocrine and non-(neuro)endocrine tumours: a comment on concepts and classification of mixed exocrine-endocrine neoplasms. Virchows Arch 2006, 449:499-506.
2. Solcia E., Kloppel G., Sobin L.H. World Health Organization international histological classification of tumors. Histological typing of endocrine tumors 2000, 56-68. Springer, Berlin, Heidelberg, New York.
3. Grimelius L. Methods in neuroendocrine histopathology. A methodological overview. Upsala J Med Sci 2008, 113:243-260.
4. Shi S.R., Key M.E., Kabra K.L. Antigen retrieval in formalin-fixed paraffin-embedded tissues: an enhancement method for immunohistochemical staining based on microwave oven heating of sections. J Histochem Cytochem 1991, 39:741-748.
5. Cattoretti G., Pileri S., Parravicini C. Antigen unmasking on formalin-fixed paraffin embedded tissue sections. J Pathol 1993, 171:83-98.
6. Frost A.R., Sparks D., Grizzle W.E. Methods of antigen recovery vary in their usefulness in unmasking specific antigens in immunohistochemistry. Appl Immunohistochem Mol Morphol 2000, 8:236-243.
7. Portela-Gomes G.M., Stridsberg M. Selective processing of chromogranin A in the different islet cells in human pancreas. J Histochem Cytochem 2001, 49:483-490.
8. Portela-Gomes G.M., Stridsberg M. Region-specific antibodies to chromogranin B display various immunostaining patterns in human endocrine pancreas. J Histochem Cytochem 2002, 50:1023-1030.
9. Portela-Gomes G.M., Stridsberg M. Chromogranin A in the human gastrointestinal tract: an immunohistochemical study with region-specific antibodies. J Histochem Cytochem 2002, 1493-1500.
10. Helle K.B. The granin family of uniquely acidic proteins of the diffuse neuroendocrine system: comparative and functional aspects. Biol Rev Camb Philos Soc 2004, 79:769-794.
11. Hagn C., Schmid K.W., Fischer-Colbrie R., Winkler H. Chromogranin A, B and C in human adrenal medulla and endocrine tissues. Lab Invest 1986, 55:405-411.
12. Taupenot L., Harper K.L., O'Connor D.T. The chromogranin-secretogranin family. N Engl J Med 2003, 348:1134-1149.
13. Banks P., Helle K. The release of protein from the stimulated adrenal medulla. Biochem J 1965, 97:40C-41C.
14. Helle K.B. Some chemical and physical properties of the soluble protein fraction of bovine adrenal chromaffin granules. Mol Pharmacol 1966, 2:298-310.
15. Deftos L.J., Hogue-Angeletti R., Chalberg C., Tu S. A chromogranin A-derived peptide differentially regulates the secretion of calcitonin gene products. J Bone Miner Res 1990, 5:989-991.
16. Drees B.M., Rouse J., Johnson J., Hamilton J.W. Bovine parathyroid glands secrete a 26-kDaN-terminal fragment of chromogranin A which inhibits parathyroid cell secretion. Endocrinology 1991, 129:3381-3387.
17. Aardal S., Helle K.B. The vasoinhibitory activity of bovine chromogranin A fragment (vasostatin) and its independence of extracellular calcium in isolated segments of human blood vessels. Regul Pept 1992, 41:9-18.
18. Corti A., Mannarino C., Mazza R., Colombo B., Longhi R., Tota B. Vasostatins exert negative inotropism in the working heart of the frog. Ann N Y Acad Sci 2002, 971:362-365.
19. Angelone T, Quintieri AM, Goumon Y, Di Felice V, Filice E, Gattuso A, Mazza R, Corti A, Tota B, Metz-Boutigue MH, Cerra MC. Cytoskeleton mediates negative inotropism and lusitropism of chromogranin A derived peptides (human vasostatin1-78 and rat CgA1-64) in the rat heart. Regul Pept 2010-this issue, http://doi:10.1016/j.regpep.2009.10.003.
20. Helle K.B. The chromogranin A-derived peptides vasostatin-I and catestatin as regulatory peptides for cardiovascular functions. Cardiovasc Res 2010, 85:9-16.
21. Lugardon K., Raffner R., Goumon Y., Corti A., Delmas A., Bulet P., Aunis D., Metz-Boutigue M.H. Antibacterial and antifungal activities of vasostatin-1, the N-terminal fragment of chromogranin A. J Biol Chem 2000, 275:10745-10753.
22. Lugardon K., Chasserot-Golaz S., Kieffer A.E., Maget-Dana R., Nullans G., Kieffer B., Aunis D., Metz-Boutigue M.H. Structural and biological characterization of chromofungin, the antifungal chromogranin A-(47-66)-derived peptide. J Biol Chem 2001, 276:35875-35882.
23. Briolat J., Wu S.D., Mahata S.K., Gonthier B., Bagnard D., Chasserot-Golaz S., Helle K.B., Aunis D., Metz-Boutigue M.-H. New antimicrobial activity for the catecholamine release-inhibitory peptide from chromogranin A. Cell Mol Life Sci 2005, 62:377-385.
24. Mahata S.K., O'Connor D.T., Mahata M., Yoo S.H., Taupenot L., Wu H., Gill B.M., Parmer R.J. Novel autocrine feedback control of catecholamine release. A discrete chromogranin A fragment is a noncompetitive nicotinic cholinergic antagonist. J Clin Invest 1997, 100:1623-1633.
25. Krüger P.G., Mahata S.K., Helle K.B. Catestatin (CgA344-364) stimulates rat mast cell release of histamine in a manner comparable to mastoparan and other cationic charged neuropeptides. Regul Pept 2003, 114:29-35.
26. Tatemoto K., Efendić S., Mutt V., Makk G., Feistner G.J., Barchas J.D. Pancreastatin, a novel pancreatic peptide that inhibits insulin secretion. Nature 1986, 324:476-478.
27. Fasciotto B.H., Trauss C.A., Greeley G.H., Cohn D.V. Parastatin (porcine chromogranin A347-419), a novel chromogranin A-derived peptide, inhibits parathyroid cell secretion. Endocrinology 1993, 133:461-466.
28. Galindo E., Rill A., Bader M.F., Aunis D. Chromostatin, a 20-amino acid peptide derived from chromogranin A, inhibits chromaffin cell secretion. Proc Natl Acad Sci USA 1991, 88:1426-1430.
29. O'Connor D.T., Burton D., Deftos L.J. Chromogranin A: immunohistology reveals its universal occurrence in normal polypeptide hormone producing endocrine glands. Life Sci 1983, 33:1657-1663.
30. O'Connor D.T., Burton D., Deftos L.J. Immunoreactive human chromogranin A in diverse polypeptide hormone producing human tumors and normal endocrine tissues. J Clin Endocrinol Metab 1983, 57:1084-1086.
31. Lloyd R.V., Wilson B.S. Specific endocrine tissue marker defined by a monoclonal antibody. Science 1983, 222:628-630.
32. Wilson B.S., Lloyd R.V. Detection of chromogranin in neuroendocrine cells with a monoclonal antibody. Am J Pathol 1984, 115:458-468.
33. Federspiel B.H., Burke A.P., Sobin L.H., Shekitha K.M. Rectal and colonic carcinoids: a clinicopathologic study of 84 cases. Cancer 1990, 65:135-140.
34. Fahrenkamp A.G., Wibbeke C., Winde G., Ofner D., Böcker W., Fischer-Colbrie R., Schmid K.W. Immunohistochemical distribution of chromogranins A and B and secretogranin II in neuroendocrine tumours of the gastrointestinal tract. Virchows Arch 1995, 426:361-367.
35. Kimura N., Pilichowska M., Okamoto H., Kimura I., Aunis D. Immunohistochemical expression of chromogranins A and B, prohormone convertases 2 and 3, and amidating enzyme in carcinoid tumors and pancreatic endocrine tumors. Mod Pathol 2000, 13:140-146.
36. Koljonen V., Haglund C., Tukiainen E., Böhling T. Neuroendocrine differentiation in primary Merkel cell carcinoma - possible prognostic significance. Anticancer Res 2005, 25:853-858.
37. Kimura N. Chromogranins in non-endocrine tumours. Adv Exp Med Biol 2000, 482:369-373.
38. Bofin A.M., Qvigstad G., Waldum C., Waldum H.L. Neuroendocrine differentiation in carcinoma of the breast. Tyramide signal amplification discloses chromogranin A-positive tumour cells in more breast tumours than previously realized. APMIS 2002, 110:658-664.
39. Makretsov N., Gilks C.B., Coldman A.J., Hayes M., Huntsman D. Tissue microarray analysis of neuroendocrine differentiation and its prognostic significance in breast cancer. Hum Pathol 2003, 34:1001-1008.
40. Moriya T., Kozuka Y., Kanomata N., Tse G.M., Tan P.H. The role of immunohistochemistry in the differential diagnosis of breast lesions. Pathology 2009, 41:68-76.
41. Kimura N., Yoshida R., Shiraishi S., Pilichowska M., Ohuchi N. Chromogranin A and chromogranin B in noninvasive and invasive breast carcinoma. Endocr Pathol 2002, 13:117-122.
42. Yoshida R., Ohuchi N., Kimura N. Clinicopathological study of chromogranin A, B and BRCA1 expression in node-negative breast carcinoma. Oncol Rep 2002, 9:1363-1367.
43. Colombo B., Curnis F., Foglieni C., Monno A., Arrigoni G., Corti A. Chromogranin A expression in neoplastic cells affects tumor growth and morphogenesis in mouse models. Cancer Res 2002, 62:941-946.
44. Abrahamsson P.A., Falkmer S., Fält K., Grimelius L. The course of neuroendocrine differentiation in prostatic carcinomas. An immunohistochemical study testing chromogranin A as an "endocrine marker". Pathol Res Pract 1989, 185:373-380.
45. Theodorescu D., Broder S.R., Boyd J.C., Mills S.E., Frierson H.F. Cathepsin D and chromogranin A as predictors of long term disease specific survival after radical prostatectomy for localized carcinoma of the prostate. Cancer 1997, 80:2109-2119.
46. Young R.H., Srigley J.R., Amin M.B., Ulbright T.M., Cubilla A.L. Carcinoma of the prostate gland (excluding unusual variants and secondary carcinomas). Atlas of Tumor Pathology 2000, vol. 28:111-216. Armed Forces Institute of Pathology, Washington DC. J. Rosai, L. Sobin (Eds.).
47. Sundaresan V., Reeve J.G., Stenning S., Stewart S., Bleehen N.M. Neuroendocrine differentiation and clinical behaviour in non-small cell lung tumours. Br J Cancer 1991, 64:333-338.
48. Gregorc V., Spreafico A., Floriani I., Colombo B., Ludovini V., Pistola L., Bellezza G., Viganò M.G., Villa E., Corti A. Prognostic value of circulating chromogranin A and soluble tumor necrosis factor receptors in advanced nonsmall cell lung cancer. Cancer 2007, 110:845-853.
49. Foley E.F., Gaffey M.J., Frierson H.F. The frequency and clinical significance of neuroendocrine cells within stage III adenocarcinomas of the colon. Arch Pathol Lab Med 1998, 122:912-914.
50. Martinsen T.C., Skogaker N.E., Fossmark R., Nordrum I.S., Sandvik A.K., Bendheim M.Ø., Bakkelund K.E., Waldum H.L. Neuroendocrine cells in diffuse gastric carcinomas: an ultrastructural study with immunogold labeling of chromogranin A. Appl Immunohistochem Mol Morphol 2010, 18:62-68.
51. Portela-Gomes G.M., Stridsberg M., Johansson H., Grimelius L. Complex co-localization of chromogranins and neurohormones in the human gastrointestinal tract. J Histochem Cytochem 1997, 45:815-822.
52. Portela-Gomes G.M., Stridsberg M., Grimelius L., Falkmer U.G., Falkmer S. Expression of chromogranins A, B, and C (secretogranin II), in human adrenal medulla and in benign and malignant pheochromocytomas. An immunohistochemical study with region-specific antibodies. APMIS 2004, 112:663-673.
53. Portela-Gomes G.M., Stridsberg M., Johansson H., Wilander E., Grimelius L. Chromogranin A in human neuroendocrine tumors: an immunohistochemical study with region-specific antibodies. Am J Surg Pathol 2001, 25:1261-1267.
54. Jin L., Zhang S., Bayliss J., Scheithauer B., Qian X., Kobayashi I., Stridsberg M., Lloyd R.V. Chromogranin a processing in human pituitary adenomas and carcinomas: analysis with region-specific antibodies. Endocr Pathol 2003, 14:37-48.
55. Lloyd R.V., Jin L., Qian X., Scheithauer B.W., Young W.F., Davis D.H. Analysis of the chromogranin A post-translational cleavage product pancreastatin and the prohormone convertases PC2 and PC3 in normal and neoplastic human pituitaries. Am J Pathol 1995, 146:1188-1198.
56. Gleeson C.M., Curry W.J., Johnston C.F., Buchanan K.D. Occurrence of WE-14 and chromogranin A-derived peptides in tissues of the human and bovine gastro-entero-pancreatic system and in human neuroendocrine neoplasia. J Endocrinol 1996, 151:409-420.
57. Hanna F.W., Ardill J.E., Johnston C.F., Cunningham R.T., Curry W.J., Russell C.F., Buchanan K.D. Regulatory peptides and other neuroendocrine markers in medullary carcinoma of the thyroid. J Endocrinol 1997, 152:275-281.
58. Cunningham R.T., Pogue K.M., Curry W.J., Johnston C.F., Sloan J.M., Buchanan K.D. Immunostaining for vasostatin I distinguishes between ileal and lung carcinoids. J Pathol 1999, 187:321-325.
59. Heaney A.P., Curry W.J., Pogue K.M., Armstrong V.L., Mirakhur M., Sheridan B., Johnston C.F., Buchanan K.D., Atkinson A.B. Immunohistochemical evaluation of the post-translational processing of chromogranin A in human pituitary adenomas. Pituitary 2000, 3:67-75.
60. Portela-Gomes G.M., Grimelius L., Stridsberg M., Puppa G., Bresaola E., Viale G., Pelosi G. Expression of amino acid sequences of the chromogranin A molecule and synaptic vesicle protein 2 in neuroendocrine tumours of the lung. Virchows Arch 2005, 446:604-612.
61. Tartaglia A., Portela-Gomes G.M., Öberg K., Vezzadini P., Foschini M.P., Stridsberg M. Chromogranin A in gastric neuroendocrine tumours: an immunohistochemical and biochemical study with region-specific antibodies. Virchows Arch 2006, 448:399-406.
62. Winkler H., Laslop A., Leitner B., Weiss C. The secretory cocktail of adrenergic large dense-core vesicles: the functional role of the chromogranins. Adv Pharmacol 1998, 42:257-259.
63. Lee R.W., Huttner W.B. Tyrosine-O-sulfated proteins of PC12 pheochromocytoma cells and their sulfation by a tyrosylprotein sulfotransferase. J Biol Chem 1983, 258:11326-11334.
64. Strub J.M., Garcia-Sablone P., Lonning K., Taupenot L., Hubert P., Van Dorsselaer A., Aunis D., Metz-Boutigue M.H. Processing of chromogranin B in bovine adrenal medulla. Identification of secretolytin, the endogenous C-terminal fragment of residues 614-626 with anti-bacterial activity. Eur J Biochem 1995, 229:356-368.
65. Metz-Boutigue M.H., Goumon Y., Strub J.M., Aunis D. Antibacterial peptides are present in chromaffin cell secretory granules. Cell Mol Neurobiol 1998, 18:249-266.
66. Karlsson E., Stridsberg M., Sandler S. Chromogranin B regulation of IAPP and insulin secretion. Regul Pept 2000, 87:33-39.
67. Weiler R., Feichtinger H., Schmid K.W., Fischer-Colbrie R., Grimelius L., Cedermark B., Papotti M., Bussolati G., Winkler H. Chromogranin A and B and secretogranin II in bronchial and intestinal carcinoids. Virchows Arch A Pathol Anat Histopathol 1987, 412:103-109.
68. Schmid K.W., Fischer-Colbrie R., Hagn C., Jasani B., Williams E.D., Winkler H. Chromogranin A and B and secretogranin II in medullary carcinomas of the thyroid. Am J Surg Pathol 1987, 11:551-556.
69. Weiler R., Fischer-Colbrie R., Schmid K.W., Feichtinger H., Bussolati G., Grimelius L., Krisch K., Kerl H., O'Connor D., Winkler H. Immunological studies on the occurrence and properties of chromogranin A and B and secretogranin II in endocrine tumors. Am J Surg Pathol 1988, 12:877-884.
70. Lloyd R.V., Cano M., Rosa P., Hille A., Huttner W.B. Distribution of chromogranin A and secretogranin I (chromogranin B) in neuroendocrine cells and tumors. Am J Pathol 1988, 130:296-304.
71. Wiedenmann B., Waldherr R., Buhr H., Hille A., Rosa P., Huttner W.B. Identification of gastroenteropancreatic neuroendocrine cells in normal and neoplastic human tissue with antibodies against synaptophysin, chromogranin A, secretogranin I (chromogranin B), and secretogranin II. Gastroenterology 1988, 95:1364-1374.
72. Bordi C., Yu J.Y., Baggi M.T., Davoli C., Pilato F.P., Baruzzi G., Gardini G., Zamboni G., Franzin G., Papotti M., Bussolati G. Gastric carcinoids and their precursor lesions. A histologic and immunohistochemical study of 23 cases. Cancer 1991, 67:663-672.
73. Vieau D., Rojas-Miranda A., Verley J.M., Lenne F., Bertagna X. The secretory granule peptides 7B2 and CCB are sensitive biochemical markers of neuro-endocrine bronchial tumours in man. Clin Endocrinol (Oxf) 1991, 35:319-325.
74. Schmid K.W., Brink M., Freytag G., Kirchmair R., Böcker W., Fischer-Colbrie R., Heitz P.U., Klöppel G. Expression of chromogranin A and B and secretoneurin immunoreactivity in neoplastic and nonneoplastic pancreatic alpha cells. Virchows Arch 1994, 425:127-132.
75. Tötsch M., Padberg B.C., Schröder S., Ofner D., Böcker W., Fischer-Colbrie R., Schmid K.W. Secretoneurin in bronchopulmonary carcinoids - immunohistochemical comparison with chromogranins A and B and secretogranin II. Histopathology 1995, 26:357-361.
76. Prommegger R., Obrist P., Ensinger C., Schwelberger H.G., Wolf C., Fischer-Colbrie R., Mikuz G., Bodner E. Secretoneurin in carcinoids of the appendix-immunohistochemical comparison with chromogranins A, B and secretogranin II. Anticancer Res 1998, 18:3999-4002.
77. Portela-Gomes GM, Grimelius L, Stridsberg M. Secretogranin III in human neuroendocrine tumours. A comparative immunohistochemical study with chromogranin A and B and secretogranin II. Regul Pept 2010-this issue.
78. Schmid K.W., Hittmair A., Ladurner D., Sandbichler P., Gasser R., Tötsch M. Chromogranin A and B in parathyroid tissue of cases of primary hyperparathyroidism: an immunohistochemical study. Virchows Arch A Pathol Anat Histopathol 1991, 418:295-299.
79. Lloyd R.V., Jin L., Fields K. Detection of chromogranins A and B in endocrine tissues with radioactive and biotinylated oligonucleotide probes. Am J Surg Pathol 1990, 14:35-43.
80. Lloyd R.V., Jin L., Kulig E., Fields K. Molecular approaches for the analysis of chromogranins and secretogranins. Diagn Mol Pathol 1992, 1:2-15.
81. Rosa P., Bassetti M., Weiss U., Huttner W.B. Widespread occurrence of chromogranins/secretogranins in the matrix of secretory granules of endocrinologically silent pituitary adenomas. J Histochem Cytochem 1992, 40:523-533.
82. Schmid K.W., Kröll M., Hittmair A., Maier H., Tötsch M., Gasser R., Finkenstett G., Hogue-Angeletti R., Fischer-Colbrie R. Chromogranin A and B in adenomas of the pituitary. An immunohistochemical study of 42 cases. Am J Surg Pathol 1991, 15:1072-1077.
83. Scopsi L., Sampietro G., Boracchi P., Collini P. Argyrophilia and chromogranin A and B immunostaining in patients with sporadic medullary thyroid carcinoma. A critical appraisal of their prognostic utility. J Pathol 1998, 184:414-419.
84. Pruneri G., Galli S., Rossi R.S., Roncalli M., Coggi G., Ferrari A., Simonato A., Siccardi A.G., Carboni N., Buffa R. Chromogranin A and B and secretogranin II in prostatic adenocarcinomas: neuroendocrine expression in patients untreated and treated with androgen deprivation therapy. Prostate 1998, 34:113-120.
85. Schmid K.W., Helpap B., Tötsch M., Kirchmair R., Dockhorn-Dworniczak B., Böcker W., Fischer-Colbrie R. Immunohistochemical localization of chromogranins A and B and secretogranin II in normal, hyperplastic and neoplastic prostate. Histopathology 1994, 24:233-239.
86. Rosa P., Zanini A. Characterization of adenohypophysial polypeptides by two-dimensional gel electrophoresis. II. Sulfated and glycosylated polypeptides. Mol Cell Endocrinol 1981, 24:181-193.
87. Fischer-Colbrie R., Laslop A., Kirchmair R. Secretogranin II: molecular properties, regulation of biosynthesis and processing to the neuropeptide secretoneurin. Prog Neurobiol 1995, 46:49-70.
88. Kirchmair R., Hogue-Angeletti R., Gutierrez J., Fischer-Colbrie R., Winkler H. Secretoneurin - a neuropeptide generated in brain, adrenal medulla and other endocrine tissues by proteolytic processing of secretogranin II (chromogranin C). Neuroscience 1993, 53:359-365.
89. Saria A., Troger J., Kirchmair R., Fischer-Colbrie R., Hogue-Angeletti R., Winkler H. Secretoneurin releases dopamine from rat strial slices: a biological effect of a peptide derived from secretogranin II (chromogranin C). Neuroscience 1993, 54:1-4.
90. Reinisch N., Kirchmair R., Kähler C.M., Hogue-Angeletti R., Fischer-Colbrie R., Winkler H., Wiedermann C.J. Attraction of human monocytes by the neuropeptide secretoneurin. FEBS Lett 1993, 334:41-44.
91. Anouar Y., Desmoucelles C., Yon L., Leprince J., Breault L., Gallo-Payet N., Vaudry H. Identification of a novel secretogranin II-derived peptide (SgII187-252) in adult and fetal human adrenal glands using antibodies raised against the human recombinant peptide. J Clin Endocrinol Metab 1998, 83:2944-2951.
92. Boutahricht M., Guillemot J., Montero-Hadjadje M., Bellafqih S., El Ouezzani S., Alaoui A., Yon L., Vaudry H., Anouar Y., Magoul R. Biochemical characterisation and immunohistochemical localisation of granin II-derived peptide EM66 in the hypothalamus of the jerboa (Jaculus orientalis): modulation by food deprivation. J Neuroendocrinol 2005, 17:372-378.
93. Vallet V.S., Li J.Y., Duval J. Secretogranin II (SgII) distribution and processing studies in human normal and adenomatous anterior pituitaries using new polyclonal antibodies. Regul Pept 1997, 68:155-163.
94. Le Gall F., Vallet V.S., Thomas D., De Monti M., Duval J., Ramee M.P. Immunohistochemical study of secretogranin II in 62 neuroendocrine tumours of the digestive tract and of the pancreas in comparison with other granins. Pathol Res Pract 1997, 193:179-185.
95. Thompson L.D.R. Pheochromocytoma of the adrenal gland scaled score (PASS) to separate benign from malignant neoplasms. A clinicopathologic and immunophenotypic study of 100 cases. Am J Surg Pathol 2002, 26:551-566.
96. Yon L., Guillemot J., Montero-Hadjadje M., Grumolato L., Leprince J., Lefebvre H., Contesse V., Plouin P.F., Vaudry H., Anouar Y. Identification of the secretogranin II-derived peptide EM66 in pheochromocytomas as a potential marker for discriminating benign versus malignant tumors. J Clin Endocrinol Metab 2003, 88:2579-2585.
97. Ottiger H.P., Battenberg E.F., Tsou A.P., Bloom F.E., Sutcliffe J.G. 1B1075: a brain- and pituitary-specific mRNA that encodes a novel chromogranin/secretogranin-like component of intracellular vesicles. J Neurosci 1990, 10:3135-3147.
98. Rong Y.P., Liu F., Zeng L.C., Ma W.J., Wei D.Z., Han Z.G. Cloning and characterization of a novel human secretory protein: secretogranin III. Acta Biochim Biophys Sinica 2002, 34:411-417.
99. Hosaka M., Watanabe T., Sakai Y., Uchiyama Y., Takeuchi T. Identification of a chromogranin A domain that mediates binding to secretogranin III and targeting to secretory granules in pituitary cells and pancreatic beta-cells. Mol Biol Cell 2002, 13:3388-3399.
100. Hosaka M., Suda M., Sakai Y., Izumi T., Watanabe T., Takeuchi T. Secretogranin III binds to cholesterol in the secretory granule membrane as an adapter for chromogranin A. J Biol Chem 2004, 279:3627-3634.
101. Srikanta S., Krisch K., Eisenbarth G.S. Islet cell proteins defined by monoclonal islet cell antibody HISL-19. Diabetes 1986, 35:300-305.
102. Krisch K., Buxbaum P., Horvat G., Krisch I., Neuhold N., Ulrich W., Srikanta S. Monoclonal antibody HISL-19 as an immunocytochemical probe for neuroendocrine differentiation. Its application in diagnostic pathology. Am J Pathol 1986, 123:100-108.
103. Bordi C., Krisch K., Horvat G., Srikanta S. Immunocytochemical patterns of islet cell tumors as defined by the monoclonal antibody HISL-19. Am J Pathol 1988, 132:249-257.
104. Deftos L.J., Woloszczuk W., Krisch I., Horvat G., Ulrich W., Neuhold N., Braun O., Reiner A., Srikanta S., Krisch K. Medullary thyroid carcinomas express chromogranin A and a novel neuroendocrine protein recognized by monoclonal antibody HISL-19. Am J Med 1988, 85:780-784.
105. Shimizu K., Namimatsu S., Kitagawa W., Akasu H., Takatsu K., Sugisaki Y., Tanaka S. Immunohistochemical, biochemical and immunoelectron microscopic analysis of antigenic proteins on neuroendocrine cell tumors using monoclonal antibody HISL-19. J Nippon Med Sch 2002, 69:365-372.
106. Neuhold N., Ullrich R. Secretogranin IV immunoreactivity in medullary thyroid carcinoma: an immunohistochemical study of 62 cases. Virchows Arch A Pathol Anat Histopathol 1993, 423:85-89.
107. Azzoni C., D'Adda T., Tamburrano G., Coscelli C., Madsen O.D., Scopsi L., Bordi C. Functioning human insulinomas. An immunohistochemical analysis of intracellular insulin processing. Virchows Arch 1998, 433:495-504.
108. Hsi K.L., Seidah N.G., De Serres G., Chrétien M. Isolation and NH2-terminal sequence of a novel porcine anterior pituitary polypeptide. Homology to proinsulin, secretin and Rous sarcoma virus transforming protein TVFV60. FEBS Lett 1982, 147:261-266.
109. Martens G.J.M. Cloning and sequence analysis of human pituitary cDNA encoding the novel polypeptide 7B2. FEBS Lett 1988, 234:160-164.
110. Ayoubi T.A., van Duijnhoven H.L., van de Ven W.J., Jenks B.G., Roubos E.W., Martens G.J. The neuroendocrine polypeptide 7B2 is a precursor protein. J Biol Chem 1990, 265:15644-15647.
111. Sigafoos J., Chestnut W.G., Merrill B.M., Taylor L.C.E., Diliberto E.J., Viveros O.H. Novel peptides from adrenomedullary chromaffin vesicles. J Anat 1993, 183:253-264.
112. Paquet L., Bergeron F., Boudreault A., Seidah N.G., Chretien M., Mbikay M., Lazure C. The neuroendocrine precursor 7B2 is a sulfated protein proteolytically processed by a ubiquitous furin-like convertase. J Biol Chem 1994, 269:19279-19285.
113. Azzoni C., Yu J.Y., Baggi M.T., D'Adda T., Timson C., Polak J.M., Bordi C. Studies on co-localization of 7B2 and pancreatic hormones in normal and tumoural islet cells. Virchows Arch A Pathol Anat Histopathol 1992, 421:457-466.
114. Iguchi H., Yasuda D., Yamada Y., Funakoshi A., Wakasugi H., Bloom S.R., Chretien M. 7B2, a possible marker for nonfunctioning pancreatic islet cell tumor. Horm Metab Res 1991, 23:486-489.
115. Zhu X., Lindberg I. 7B2 facilitates the maturation of proPC2 in neuroendocrine cells and is required for the expression of enzymatic activity. J Cell Biol 1995, 129:1641-1650.
116. Suzuki H., Ghatei M.A., Williams S.J., Uttenthal L.O., Facer P., Bishop A.E., Polak J.M., Bloom S.R. Production of pituitary protein 7B2 immunoreactivity by endocrine tumors and its possible diagnostic value. J Clin Endocrinol Metab 1986, 63:758-765.
117. Marcinkiewicz M., Benjannet S., Falgueyret J.P., Seidah N.G., Schürch W., Verdy M., Cantin M., Chrétien M. Identification and localization of 7B2 protein in human, porcine, and rat thyroid gland and in human medullary carcinoma. Endocrinology 1988, 123:866-873.
118. Ischia R., Lovisetti-Scamihorn P., Hogue-Angeletti R., Wolkersdorfer M., Winkler H., Fischer-Colbrie R. Molecular cloning and characterization of NESP55, a novel chromogranin-like precursor of a peptide with 5-HT1B receptor antagonist activity. J Biol Chem 1997, 272:11657-11662.
119. Weiss U., Ischia R., Eder S., Lovisetti-Scamihorn P., Bauer R., Fischer-Colbrie R. Neuroendocrine secretory protein 55 (NESP55): alternative splicing onto transcripts of the GNAS gene and posttranslational processing of a maternally expressed protein. Neuroendocrinology 2000, 71:177-186.
120. Rousselle J.C., Massot O., Delepierre M., Zifa E., Rousseau B., Fillion G. Isolation and characterization of an endogenous peptide from rat brain interacting specifically with the serotonergic 1B receptor subtypes. J Biol Chem 1996, 271:726-735.
121. Jakobsen A.M., Ahlman H., Kölby L., Abrahamsson J., Fischer-Colbrie R., Nilsson O. NESP55, a novel chromogranin-like peptide, is expressed in endocrine tumours of the pancreas and adrenal medulla but not in ileal carcinoids. Br J Cancer 2003, 88:1746-1754.
122. Srivastava A., Padilla O., Fischer-Colbrie R., Tischler A.S., Dayal Y. Neuroendocrine secretory protein-55 (NESP-55) expression discriminates pancreatic endocrine tumors and pheochromocytomas from gastrointestinal and pulmonary carcinoids. Am J Surg Pathol 2004, 28:1371-1378.
123. Srivastava A., Hornick J.L. Immunohistochemical staining for CDX-2, PDX-1, NESP-55, and TTF-1 can help distinguish gastrointestinal carcinoid tumors from pancreatic endocrine and pulmonary carcinoid tumors. Am J Surg Pathol 2009, 33:626-632.
124. Levi A., Eldridge J.D., Paterson B.M. Molecular cloning of a gene sequence regulated by nerve growth factor. Science 1985, 229:393-395.
125. Twardzik D.R., Brown J.P., Ranchalis J.E., Todaro G.J., Moss B. Vaccinia virus-infected cells release a novel polypeptide functionally related to transforming and epidermal growth factors. Proc Natl Acad Sci USA 1985, 82:5300-5304.
126. Trani E., Rinaldi A.M., Canu N., Ciotti M.T., Ferri G.L., Levi A., Possenti R. Tissue-specific processing of neuroendocrine protein VGF. J Neurochem 1995, 65:2441-2449.
127. Possenti R., Rinaldi A.M., Ferri G.L., Borboni P., Trani E., Levi A. Expression, processing and secretion of the neuroendocrine VGF peptides by INS-1 cells. Endocrinol 1999, 140:3727-3735.
128. Toshinai K., Nakazato M. Neuroendocrine regulatory peptide-1 and -2: novel bioactive peptides processed from VGF. Cell Mol Life Sci 2009, 66:1939-1945.
129. Taylor J.M., Quilty D., Banadyga L., Barry M. The vaccinia virus protein F1L interacts with Bim and inhibits activation of the pro-apoptotic protein Bax. J Biol Chem 2006, 281:39728-39739.
130. Postigo A., Martin M.C., Dodding M.P., Way M. Vaccinia-induced epidermal growth factor receptor-MEK signalling and the anti-apoptotic protein F1L synergize to suppress cell death during infection. Cell Microbiol 2009, 11:1208-1218.
131. Rindi G., Licini L., Necchi V., Bottarelli L., Campanini N., Azzoni C., Favret M., Giordano G., D'Amato F., Brancia C., Solcia E., Ferri G.L. Peptide products of the neurotrophin-inducible gene vgf are produced in human neuroendocrine cells from early development and increase in hyperplasia and neoplasia. J Clin Endocrinol Metab 2007, 92:2811-2815.
132. Biswas N., Rodriguez-Flores J.L., Courel M., Gayen J.R., Vaingankar S.M., Mahata M., Torpey J.W., Taupenot L., O'Connor D.T., Mahata S.K. Cathepsin L co-localizes with chromogranin A in chromaffin vesicles to generate active peptides. Endocrinology 2009, 150:3547-3557.
133. Zhou A., Webb G., Zhu X., Steiner D.F. Proteolytic processing in the secretory pathway. J Biol Chem 1999, 274:20745-20748.
134. Hook V., Funkelstein L., Lu D., Bark S., Wegrzyn J., Hwang S.R. Proteases for processing proneuropeptides into peptide neurotransmitters and hormones. Annu Rev Pharmacol Toxicol 2008, 48:393-423.
135. Parmer R.J., Mahata M., Gong Y., Mahata S.K., Jiang Q., O'Connor D.T., Xi X.P., Miles L.A. Processing of chromogranin A by plasmin provides a novel mechanism for regulating catecholamine secretion. J Clin Invest 2000, 106:907-915.
136. Jiang Q., Taupenot L., Mahata S.K., Mahata M., O'Connor D.T., Miles L.A., Parmer R.J. Proteolytic cleavage of chromogranin A (CgA) by plasmin. Selective liberation of a specific bioactive CgA fragment that regulates catecholamine release. J Biol Chem 2001, 276:25022-25029.
137. Eipper B.A., Stoffers D.A., Mains R.E. The biosynthesis of neuropeptides: peptide alpha-amidation. Annu Rev Neurosci 1992, 15:57-85.
138. Steel J.H., Martínez A., Springall D.R., Treston A.M., Cuttitta F., Polak J.M. Peptidylglycine alpha-amidating monooxygenase (PAM) immunoreactivity and messenger RNA in human pituitary and increased expression in pituitary tumours. Cell Tissue Res 1994, 276:197-207.
139. Saldise L., Martínez A., Montuenga L.M., Treston A., Springall D.R., Polak J.M., Vázquez J.J. Distribution of peptidyl-glycine alpha-amidating mono-oxygenase (PAM) enzymes in normal human lung and in lung epithelial tumors. J Histochem Cytochem 1996, 44:3-12.
140. Seidah N.G., Chrétien M. Proprotein and prohormone convertases: a family of subtilases generating diverse bioactive polypeptides. Brain Res 1999, 27:45-62.
141. Von Eggelkraut-Gottanka R., Beck-Sickinger A.G. Biosynthesis of peptide hormones derived from precursor sequences. Curr Med Chem 2004, 11:2651-2665.
142. Scopsi L., Gullo M., Rilke F., Martin S., Steiner D.F. Proprotein convertases (PC1/PC3 and PC2) in normal and neoplastic human tissues: their use as markers of neuroendocrine differentiation. J Clin Endocrinol Metab 1995, 80:294-301.
143. Tomita T. Immunocytochemical localization of prohormone convertase 1/3 and 2 in thyroid C-cells and medullary thyroid carcinomas. Endocr Pathol 2000, 11:165-172.
144. Tomita T. Immunocytochemical localization of prohormone convertase 1/3 and 2 in pancreatic islet cells and islet cell tumors. Pancreas 2001, 23:172-176.
145. Tomita T. Immunocytochemical localization of prohormone convertase 1/3 and 2 in gastrointestinal carcinoids. Endocr Pathol 2001, 12:137-145.
146. Kajiwara H., Itoh Y., Itoh J., Yasuda M., Osamura R.Y. Immunohistochemical expressions of prohormone convertase (PC)1/3 and PC2 in carcinoids of various organs. Tokai J Exp Clin Med 1999, 24:13-20.
147. Takumi I., Steiner D.F., Sanno N., Teramoto A., Osamura R.Y. Localization of prohormone convertases 1/3 and 2 in the human pituitary gland and pituitary adenomas: analysis by immunohistochemistry, immunoelectron microscopy, and laser scanning microscopy. Mod Pathol 1998, 11:232-238.
148. Fricker L.D., McKinzie A.A., Sun J., Curran E., Qian Y., Yan L., Patterson S.D., Courchesne P.L., Richards B., Levin N., Mzhavia N., Devi L.A., Douglass J. Identification and characterization of proSAAS, a granin-like neuroendocrine peptide precursor that inhibits prohormone processing. J Neurosci 2000, 20:639-648.
149. Zhong M., Munzer J.S., Basak A., Benjannet S., Mowla S.J., Decroly E., Chrétien M., Seidah N.G. The prosegments of furin and PC7 as potent inhibitors of proprotein convertases. In vitro and ex vivo assessment of their efficacy and selectivity. J Biol Chem 1999, 274:33913-33920.
150. Basak A. Inhibitors of proprotein convertases. J Mol Med 2005, 83:844-855.
151. Hook V.Y., Purviance R.T., Azaryan A.V., Hubbard G., Krieger T.J. Purification and characterization of alpha 1-antichymotrypsin-like protease inhibitor that regulates prohormone thiol protease involved in enkephalin precursor processing. J Biol Chem 1993, 268:20570-20577.
152. Hook V.Y., Hwang S.R. Novel secretory vesicle serpins, endopin 1 and endopin 2: endogenous protease inhibitors with distinct target protease specificities. Biol Chem 2002, 383:1067-1074.
153. Hook V.Y., Yasothornsrikul S., Hwang S.R. Novel chromaffin granule serpins, endopin 1 and endopin 2: endogenous protease inhibitors with distinct target protease specificities. Ann N Y Acad Sci 2002, 971:426-444.
154. de Koning P.J., Bovenschen N., Broekhuizen R., Lips C.J., Kummer J.A. Serine protease inhibitor 8 is a novel immunohistochemical marker for neuroendocrine tumors of the pancreas. Pancreas 2009, 38:461-467.
155. Khatib A.M., Siegfried G., Chrétien M., Metrakos P., Seidah N.G. Pro-protein convertases in tumor progression and malignancy: novel targets in cancer therapy. Am J Pathol 2002, 160:1921-1935.
156. Scamuffa N., Siegfried G., Bontemps Y., Ma L., Basak A., Cherel G., Calvo F., Seidah N.G., Khatib A.M. Selective inhibition of proprotein convertases represses the metastatic potential of human colorectal tumor cells. J Clin Invest 2008, 118:352-363.
157. Coppola J.M., Bhojani M.S., Ross B.D., Rehemtulla A. A small-molecule furin inhibitor inhibits cancer cell motility and invasiveness. Neoplasia 2008, 10:363-370.
158. Komiyama T., Coppola J.M., Larsen M.J., van Dort M.E., Ross B.D., Day R., Rehemtulla A., Fuller R.S. Inhibition of furin/proprotein convertase-catalyzed surface and intracellular processing by small molecules. J Biol Chem 2009, 284:15729-15738.