Progesterone regulates the expression and activity of two mouse isoforms of the glycoprotein folding sensor UDP-Glc: Glycoprotein glucosyltransferase (UGGT)

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 12, 2013, Pages 3368-3374

  Prados, María B ^a   Caramelo, Julio J ^a   Miranda, Silvia E ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

DJN; Endoplasmic reticulum quality control; Folding; P4; Progesterone; UDP Glc: glycoprotein glucosyltransferase; UGGT; UPR

Indexed keywords

GLUCOSYLTRANSFERASE; GLYCOPROTEIN; PROGESTERONE; UDP GLUCOSE GLYCOPROTEIN GLUCOSYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; GENE EXPRESSION; GENE SILENCING; HORMONAL REGULATION; HYBRIDOMA; HYBRIDOMA CELL CULTURE; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN SYNTHESIS; QUALITY CONTROL; UNFOLDED PROTEIN RESPONSE;

EID: 84886822755     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.09.022     Document Type: Article

References (53)

1. Helenius A., Aebi M. Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 2004, 73:1019-1049.
2. Hebert D.N., Garman S.C., Molinari M. The glycan code of the endoplasmic reticulum: asparagine-linked carbohydrates as protein maturation and quality-control tags. Trends Cell Biol. 2005, 15(7):364-370.
3. D'Alessio C., Caramelo J., Parodi A. UDP-Glc:glycoprotein glucosyltransferase-glucosidase II the ying-yang of the ER quality control. Semin. Cell Dev. Biol. 2010, 21-5:491-499.
4. Kornfeld R., Kornfeld S. Assembly of asparagine linked oligosaccharides. Annu. Rev. Biochem. 1985, 54:631-664.
5. Caramelo J.J., Castro O.A., Alonso L.G., de Prat-Gay G., Parodi A.J. UDPGlc:glycoprotein glucosyltransferase recognizes structured and solvent accessible hydrophobic patches in molten globule-like folding intermediates. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:86-91.
6. Caramelo J.J., Castro O.A., de Prat-Gay G., Parodi A.J. The endoplasmic reticulum glucosyltransferase recognizes nearly native glycoprotein folding intermediates. J. Biol. Chem. 2004, 279:46280-46285.
7. Keith N., Parodi A.J., Caramelo J.J. Glycoprotein tertiary and quaternary structures are monitored by the same quality control mechanism. J. Biol. Chem. 2005, 280:18138-18141.
8. Cabral C.M., Liu Y., Sifers R.N. Dissecting glycoprotein quality control in the secretory pathway. Trends Biochem. Sci. 2001, 26:619-624.
9. Brodsky J.L. Cleaning up: ER-associated degradation to the rescue. Cell 2012, 151:1163-1167.
10. Schröder M., Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 2005, 74:739-789.
11. Arnold S.M., Fessler L., Fessler J., Kaufman R. Two homologues encoding human UDP-Glucose:Glycoprotein Glucosyltransferase differ in mRNA expression and enzymatic activity. Biochemistry 2000, 39:2149-2163.
12. Lecca M.R., Wagner U., Patrignani A., Berger E.G., Hennet T. Genome-wide analysis of the unfolded protein response in fibroblasts from congenital disorders of glycosylation type-I patients. FASEB J. 2004, 19(2):240-242.
13. Hotamisligil G.S. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010, 140:900-917.
14. Zhang K., Wong H.N., Song B., Miller C.N., Scheuner D., Kaufman R.J. The unfolded protein response sensor IRE1alpha is required at 2 distinct steps in B cell lymphopoiesis. J. Clin. Invest. 2005, 115:268-281.
15. Moore K.A., Hollien J. The unfolded protein response in secretory cell function. Annu. Rev. Genet. 2012, 46:165-183.
16. Zhang K., Kaufman R.J. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008, 454:455-462.
17. Cornejo V.H., Hetz C. The unfolded protein response in Alzheimer's disease. Semin. Immunopathol. 2013, 35(3):277-292.
18. Hughes G.C. Progesterone and autoimmune disease. Autoimmun. Rev. 2012, 11(6,7):A502-A514.
19. Thomas P., Pang Y. Protective actions of progesterone in the cardiovascular system: potential role of membrane progesterone receptors (mPRs) in mediating rapid effects. Steroids 2013, 78:583-588.
20. Giatti S., Boraso M., Melcangi R.C., Viviani B. Neuroactive steroids, their metabolites, and neuroinflammation. J. Mol. Endocrinol. 2012, 49:125-134.
21. Oettel M., Mukhopadhyay A.K. Progesterone: the forgotten hormone in men?. Aging Male 2004, 7(3):236-257.
22. Cekic M., Johnson S., Bhatt V., Stein D. Progesterone treatment alters neurotrophin/proneurotrophin balance and receptor expression in rats with traumatic brain injury. Restor. Neurol. Neurosci. 2012, 30(2):115-126.
23. Fahnestock M., Michalski B., Xu B., Coughlin M.D. The precursor pro-nerve growth factor is the predominant form of nerve growth factor in brain and is increased in Alzheimer's disease. Mol. Cell. Neurosci. 2001, 18(2):210-220.
24. Goodman Y., Bruce A.J., Cheng B., Mattson M.P. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons. Neurochemistry 1996, 66(5):1836-1844.
25. Dioufa N., Kassi E., Papavassiliou A.G., Kiaris H. Atypical induction of the unfolded protein response by mifepristone. Endocrine 2010, 38:167-173.
26. Soares M.J., Talamantes F. Gestational effects on placental and serum androgen, progesterone and prolactin-like activity in the mouse. J. Endocrinol. 1982, 95(1):29-36.
27. Stites D.P., Siiteri P.K. Steroids as immunosuppressants in pregnancy. Immunol. Rev. 1983, 75:117-138.
28. Osman R.A., Andria M.L., Jones D.A., Meizel S. Steroid induced exocytosis: the human sperm acrosome reaction. Biochem. Biophys. Res. Commun. 1989, 160:828-833.
29. Khan-Dawood F.S., Goldsmith L.T., Weiss G., Dawood M.Y. Human corpus luteum secretion of relaxin, oxytocin, and progesterone. J. Clin. Endocrinol. Metab. 1989, 68:627-631.
30. Arck P., Hansen P.J., Mulac Jericevic B., Piccinni M.P., Szekeres-Bartho J. Progesterone during pregnancy: endocrine-immune cross talk in mammalian species and the role of stress. Am. J. Reprod. Immunol. 2007, 58:268-279.
31. Pelletier G. Steroidogenic enzymes in the brain: morphological aspects. Prog. Brain Res. 2010, 181:193-207.
32. Schumacher M., Hussain R., Gago N., Oudinet J.P., Mattern C., Ghoumari A.M. Progesterone synthesis in the nervous system: implications for myelination and myelin repair. Front. Neurosci. 2012, 6:10.
33. Miyaura H., Iwata M. Direct and indirect inhibition of Th1 development by progesterone and glucocorticoids. J. Immunol. 2002, 168(3):1087-1094.
34. Esteves C.S., Verza S. Relationship of in vitro acrosome reaction to sperm function: an update. Open Reprod. Sci. J. 2011, 3:72-84.
35. Morelli L., Plotkin L., Leoni J., Fossati C., Margni R. Analysis of oligosaccharides involved in the asymmetrical glycosylation of IgG monoclonal antibodies. Mol. Immunol. 1993, 30:695-700.
36. Prados M.B., LaBlunda J., Szekeres-Bartho J., Caramelo J., Miranda S. Progesterone induces a switch in oligosaccharyltransferase isoform expression: consequences on IgG N-glycosylation. Immunol. Lett. 2011, 137:28-37.
37. Trombetta S., Bosch M., Parodi A. Glucosylation of glycoproteins by mammalian plant fungal and trypanosomatid protozoa microsomal membranes. Biochemistry 1989, 28:8108-8116.
38. Finn R.D., Mistry J., Tate J., Coggill P., Heger A., Pollington J.E., Gavin O.L., Gunesekaran P., Ceric G., Forslund K., Holm L., Sonnhammer E.L., Eddy S.R., Bateman A. The Pfam protein families database. Nucleic Acids Res. Database Issues 2010, 38:D211-D222.
39. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 2000, 300:1005-1016.
40. Zuber C., Fan J.Y., Guhl B., Parodi A., Fessler J.H., Parker C., Roth J. Immunolocalization of UDP-glucose:glycoprotein glucosyltransferase indicates involvement of pre-Golgi intermediates in protein quality control. Proc. Natl. Acad. Sci. U. S. A. 11 2001, 98(19):10710-10715.
41. Arnold S.M., Kaufman R.J. The noncatalytic portion of human UDPglucose:glycoprotein glucosyltransferase I confers UDP-glucose binding and transferase function to the catalytic domain. J. Biol. Chem. 2003, 278:43320-43328.
42. Ruddock L.W., Molinari M. N-glycan processing in ER quality control. J. Cell Sci. 2006, 119:4373-4380.
43. Meunier L., Usherwood Y.K., Chung K.T., Hendershot L.M. A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol. Biol. Cell 2002, 13:4456-4469.
44. Korotkov K.V., Kumaraswamy E., Zhou Y., Hatfield D.L., Gladyshev V.N. Association between the 15-kDa selenoprotein and UDP-glucose:glycoprotein glucosyltransferase in the endoplasmic reticulum of mammalian cells. J. Biol. Chem. 4 2001, 276(18):15330-15336.
45. Buzzi L.I., Simonetta S.H., Parodi A., Castro O.A. The two Caenorhabditis elegans UDP-glucose:glycoprotein glucosyltransferase homologues have distinct biological functions. PLoS One 2011, 6(11):e27025.
46. Molinari M., Galli C., Vanoni O., Arnold S.M., y Kaufman R.J. Persistent glycoprotein misfolding activates the glucosidase II/UGT1-driven calnexin cycle to delay aggregation and loss of folding competence. Mol. Cell 2005, 20:503-512.
47. Jansen G., Määttänen P., Denisov A.Y., Scarffe L., Schade B., Balghi H., Dejgaard K., Chen L.Y., Muller W.J., Gehring K., Thomas D.Y. An interaction map of endoplasmic reticulum chaperones and foldases. Mol. Cell. Proteomics 2012 Sep, 11(9):710-723.
48. Canellada A., Blois S., Gentile T., Margni R. In vitro modulation of protective antibody responses by estrogen, progesterone and interleukin-6. Am. J. Reprod. Immunol. 2002, 47:8735-8920.
49. Thomas P. Characteristics of membrane progestin receptor alpha (mPRα) and progesterone membrane receptor component one (PGMRC1) and their roles in mediating rapid progestin actions. Front. Neuroendocrinol. 2008, 29(2):292-312.
50. Thomas P. Rapid steroid hormone actions initiated at the cell surface and the receptors that mediate them with an emphasis on recent progress in fish models. Gen. Comp. Endocrinol. 2012, 175:367-383.
51. Smith J.L., Kupchak B.R., Garitaonandia I., Hoang L.K., Maina A.S., Regalla L.M., Lyons T.J. Heterologous expression of human mPRalpha, mPRbeta and mPRgamma in yeast confirms their ability to function as membrane progesterone receptors. Steroids 2008, 73:1160-1173.
52. Ndiaye K., Poole D.H., Walusimbi S., Cannon M.J., Toyokawa K., Maalouf S.W., Dong J., Thomas P., Pate J.L. Progesterone effects on lymphocytes may be mediated by membrane progesterone receptors. J. Reprod. Immunol. 2012, 95:15-26.
53. Feige M.J., Groscurth S., Marcinowski M., Shimizu Y., Kessler H., Hendershot L.M., Buchner J. An unfolded CH1 domain controls the assembly and secretion of IgG antibodies. Mol. Cell 2009, 34(5):569-579.