Carboxypeptidase e and secretogranin III coordinately facilitate efficient sorting of proopiomelanocortin to the regulated secretory pathway in AtT20 cells

Molecular Endocrinology

Volumn 30, Issue 1, 2016, Pages 37-47

  Cawley, Niamh X ^a   Rathod, Trushar ^a   Young, Sigrid ^a   Lou, Hong ^a   Birch, Nigel ^b   Peng Loh, Y ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYPEPTIDASE H; CHROMOGRANIN; CHROMOGRANIN A; CORTICOTROPIN; HORMONE PRECURSOR; PEPTIDE HORMONE; PROOPIOMELANOCORTIN; RNA; SECRETOGRANIN III; SYNTAXIN; SYNTAXIN 6; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; CORTICOTROPIN RELEASE; DOWN REGULATION; GENE SILENCING; HORMONE PROTEIN COMPLEX; HORMONE RELEASE; IMMUNOCYTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SECRETORY GRANULE; SUCROSE DENSITY GRADIENT CENTRIFUGATION; TRANS GOLGI NETWORK; ACTH SECRETING CELL; ANIMAL; CELL LINE; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; RNA INTERFERENCE; SECRETORY PATHWAY; SECRETORY VESICLE;

ANIMALS; CARBOXYPEPTIDASE H; CELL LINE; CHROMOGRANINS; CORTICOTROPHS; MICE; PRO-OPIOMELANOCORTIN; PROTEIN TRANSPORT; RNA INTERFERENCE; SECRETORY PATHWAY; SECRETORY VESICLES;

EID: 84953293757     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2015-1166     Document Type: Article

References (38)

1. Thiele C, Huttner WB. The disulfide-bonded loop of chromogranins, which is essential for sorting to secretory granules, mediates homodimerization. J Biol Chem. 1998;273:1223-1231.
2. Glombik MM, Krömer A, Salm T, Huttner WB, Gerdes HH. The disulfide-bonded loop of chromogranin B mediates membrane binding and directs sorting from the trans-Golgi network to secre-tory granules. EMBO J. 1999;18:1059-1070.
3. Lou H, Kim SK, Zaitsev E, Snell CR, Lu B, Loh YP. Sorting and activity-dependent secretion of BDNF require interaction of a specific motif with the sorting receptor carboxypeptidase e. Neuron. 2005;45:245-255.
4. Loh YP, Maldonado A, Zhang C, Tam WH, Cawley N. Mechanism of sorting proopiomelanocortin and proenkephalin to the regulated secretory pathway of neuroendocrine cells. Ann NY Acad Sci. 2002; 971:416-425.
5. Dhanvantari S, Shen FS, Adams T, et al. Disruption of a receptor-mediated mechanism for intracellular sorting of proinsulin in familial hyperproinsulinemia. Mol Endocrinol. 2003;17:1856-1867.
6. Cool DR, Normant E, Shen F, et al. Carboxypeptidase E is a regulated secretory pathway sorting receptor: genetic obliteration leads to endocrine disorders in Cpe(fat) mice. Cell. 1997;88:73-83.
7. Tam WW, Andreasson KI, Loh YP. The amino-terminal sequence of pro-opiomelanocortin directs intracellular targeting to the regulated secretory pathway. Eur J Cell Biol. 1993;62:294-306.
8. Cool DR, Loh YP. Carboxypeptidase E is a sorting receptor for prohormones: binding and kinetic studies. Mol Cell Endocrinol. 1998;139:7-13.
9. Dhanvantari S, Loh YP. Lipid raft association of carboxypeptidase E is necessary for its function as a regulated secretory pathway sorting receptor. J Biol Chem. 2000;275:29887-29893.
10. Dhanvantari S, Arnaoutova I, Snell CR, et al. Carboxypeptidase E, a prohormone sorting receptor, is anchored to secretory granules via a C-terminal transmembrane insertion. Biochemistry. 2002;41: 52-60.
11. Shen FS, Loh YP. Intracellular misrouting and abnormal secretion of adrenocorticotropin and growth hormone in cpefat mice associated with a carboxypeptidase E mutation. Proc Natl Acad Sci USA. 1997;94:5314-5319.
12. Hosaka M, Watanabe T, Sakai Y, Kato T, Takeuchi T. Interaction between secretogranin III and carboxypeptidase E facilitates prohormone sorting within secretory granules. J Cell Sci. 2005;118: 4785-4795.
13. Bartolomucci A, Possenti R, Mahata SK, Fischer-Colbrie R, Loh YP, Salton SR. The extended granin family: structure, function, and biomedical implications. Endocr Rev. 2011;32:755-797.
14. 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-cells. Mol Biol Cell. 2002;13:3388-3399.
15. Hosaka M, Suda M, Sakai Y, Izumi T, Watanabe T, Takeuchi T. Secretogranin III binds to cholesterol in the secretory granule mem-brane as an adapter for chromogranin A. J Biol Chem. 2004;279: 3627-3634.
16. Montero-Hadjadje M, Elias S, Chevalier L, et al. Chromogranin A promotes peptide hormone sorting to mobile granules in constitutively and regulated secreting cells: role of conserved N-and C-terminal peptides. J Biol Chem. 2009;284:12420-12431.
17. Sun M, Watanabe T, Bochimoto H, et al. Multiple sorting systems for secretory granules ensure the regulated secretion of peptide hormones. Traffic. 2013;14:205-218.
18. Koshimizu H, Cawley NX, Kim T, Yergey AL, Loh YP. Serpinin: a novel chromogranin A-derived, secreted peptide up-regulates protease nexin-1 expression and granule biogenesis in endocrine cells. Mol Endocrinol. 2011;25:732-744.
19. Cawley NX, Rodriguez YM, Maldonado A, Loh YP. Trafficking of mutant carboxypeptidase E to secretory granules in a-cell line derived from Cpe(fat)/Cpe(fat) mice. Endocrinology. 2003;144: 292-298.
20. Zhu YL, Conway-Campbell B, Waters MJ, Dannies PS. Prolonged retention after aggregation into secretory granules of human R183H-growth hormone (GH), a mutant that causes autosomal dominant GH deficiency type II. Endocrinology. 2002;143:4243-4248.
21. Gabbay KH, DeLuca K, Fisher JN Jr., Mako ME, Rubenstein AH. Familial hyperproinsulinemia. An autosomal dominant defect. N Engl J Med. 1976;294:911-915.
22. Pivonello R, De Martino MC, De Leo M, Lombardi G, Colao A. Cushing’s syndrome. Endocrinol Metab Clin North Am. 2008;37: 135-149, ix.
23. Canaff L, Bennett HP, Hendy GN. Peptide hormone precursor processing: getting sorted? Mol Cell Endocrinol. 1999;156:1-6.
24. Dikeakos JD, Reudelhuber TL. Sending proteins to dense core secretory granules: still a lot to sort out. J Cell Biol. 2007;177:191-196.
25. Chanat E, Huttner WB. Milieu-induced, selective aggregation of regulated secretory proteins in the trans-Golgi network. J Cell Biol. 1991;115:1505-1519.
26. Seksek O, Biwersi J, Verkman AS. Direct measurement of trans-Golgi pH in living cells and regulation by second messengers. J Biol Chem. 1995;270:4967-4970.
27. Rindler MJ, Colomer V, Jin Y. Immature granules are not major sites for segregation of constitutively secreted granule content proteins in NIT-1 insulinoma cells. Biochem Biophys Res Commun. 2001;288:1071-1077.
28. Bloomquist BT, Eipper BA, Mains RE. Prohormone-converting enzymes: regulation and evaluation of function using antisense RNA. Mol Endocrinol. 1991;5:2014-2024.
29. Zhou A, Bloomquist BT, Mains RE. The prohormone convertases PC1 and PC2 mediate distinct endoproteolytic cleavages in a strict temporal order during proopiomelanocortin biosynthetic processing. J Biol Chem. 1993;268:1763-1769.
30. Matlin KS, Simons K. Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation. Cell. 1983;34:233-243.
31. Zhou A, Mains RE. Endoproteolytic processing of proopiomelano-cortin and prohormone convertases 1 and 2 in neuroendocrine cells overexpressing prohormone convertases 1 or 2. J Biol Chem. 1994; 269:17440-17447.
32. Zhou Y, Lindberg I. Enzymatic properties of carboxyl-terminally truncated prohormone convertase 1 (PC1/SPC3) and evidence for autocatalytic conversion. J Biol Chem. 1994;269:18408-18413.
33. Friedman TC, Loh YP, Birch NP. In vitro processing of proopio-melanocortin by recombinant PC1 (SPC3). Endocrinology. 1994; 135:854-862.
34. Kemppainen RJ, Behrend EN. Acute inhibition of carboxypeptidase E expression in AtT-20 cells does not affect regulated secretion of ACTH. Regul Pept. 2010;165:174-179.
35. Aoki Y, Iwasaki Y, Katahira M, Oiso Y, Saito H. Regulation of the rat proopiomelanocortin gene expression in AtT-20 cells. I: effects of the common secretagogues. Endocrinology. 1997;138:1923-1929.
36. Tsukamoto N, Otsuka F, Miyoshi T, et al. Effects of bone morphogenetic protein (BMP) on adrenocorticotropin production by pituitary corticotrope cells: involvement of up-regulation of BMP re-ceptor signaling by somatostatin analogs. Endocrinology. 2010; 151:1129-1141.
37. Tsukamoto N, Otsuka F, Ogura-Ochi K, et al. Melatonin receptor activation suppresses adrenocorticotropin production via BMP-4 action by pituitary AtT20 cells. Mol Cell Endocrinol. 2013;375: 1-9.
38. Arnaoutova I, Cawley NX, Patel N, Kim T, Rathod T, Loh YP. Aquaporin 1 is important for maintaining secretory granule bio-genesis in endocrine cells. Mol Endocrinol. 2008;22:1924-1934.