Luteinizing hormone receptor ectodomain splice variant misroutes the full-length receptor into a subcompartment of the endoplasmic reticulum

Molecular Biology of the Cell

Volumn 17, Issue 5, 2006, Pages 2243-2255

  Apaja, Pirjo M ^a   Tuusa, Jussi T ^a   Pietilä, E Maritta ^a   Rajaniemi, Hannu J ^a   Petäjä Repo, Ulla E ^a  

^a UNIVERSITY OF OULU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

CALNEXIN; CALRETICULIN; CELL SURFACE RECEPTOR; CHAPERONE; G PROTEIN COUPLED RECEPTOR; LACTACYSTIN; LUTEINIZING HORMONE RECEPTOR; MESSENGER RNA; TETRACYCLINE;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN HEK293; CELL SURFACE; CONTROLLED STUDY; CYTOSOL; ECTODOMAIN SPLICE VARIANT; ENDOPLASMIC RETICULUM; HORMONE BINDING; HORMONE RECEPTOR INTERACTION; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; QUALITY CONTROL; RAT;

ACETYLCYSTEINE; ALTERNATIVE SPLICING; CALNEXIN; CALRETICULIN; CELLS, CULTURED; CHORIONIC GONADOTROPIN; CYSTEINE PROTEINASE INHIBITORS; ENDOPLASMIC RETICULUM; HUMANS; MOLECULAR CHAPERONES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; RECEPTORS, LH;

EID: 33744923745     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-09-0875     Document Type: Article

References (58)

1. Aatsinki, J. T., Pietilä, E. M., Lakkakorpi, J. T., and Rajaniemi, H. J. (1992). Expression of the LH/CG receptor gene in rat ovarian tissue is regulated by an extensive alternative splicing of the primary transcript. Mol. Cell. Endocrinol. 84, 127-135.
2. Aatsinki, J. T., and Rajaniemi, H. J. (2005). An alternative use of basic pGEX vectors for producing N- and C-terminal fusion proteins for production and affinity purification of antibodies. Protein Expr. Purif. 40, 287-291.
3. Apaja, P. M., Aatsinki, J. T., Rajaniemi, H. J., and Petäjä- Repo, U. E. (2005). Expression of the mature luteinizing hormone receptor in rodent urogenital and adrenal tissues is developmentally regulated at a posttranslational level. Endocrinology 146, 3224-3232.
4. Apaja, P. M., Harju, K. T., Aatsinki, J. T., Petäjä-Repo, U. E., and Rajaniemi, H. J. (2004). Identification and structural characterization of the neuronal luteinizing hormone receptor associated with sensory systems. J. Biol. Chem. 279, 1899-1906.
5. Ascoli, M., Fanelli, F., and Segaloff, D. L. (2002). The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr. Rev. 23, 141-174.
6. Bebök, Z., Mazzochi, C., King, S. A., Hong, J. S., and Sorscher, E. J. (1998). The mechanism underlying cystic fibrosis transmembrane conductance regulator transport from the endoplasmic reticulum to the proteasome includes Sec61β and a cytosolic, deglycosylated intermediary. J. Biol. Chem. 273, 29873-29878.
7. Benkirane, M., Jin, D. Y., Chun, R. F., Koup, R. A., and Jeang, K. T. (1997). Mechanism of transdominant inhibition of CCR5-mediated HIV-1 infection by ccr5δ32. J. Biol. Chem. 272, 30603-30606.
8. Bozon, V., Couture, L., Pajot-Augy, E., Richard, F., Remy, J. J., and Salesse, R. (2002). Rescue of intracellularly trapped lutropin receptor exodomain by endodomain and reconstitution of a functional membrane receptor: interaction between exo- and endodomains. Protein Expr. Purif. 25, 114-123.
9. Braun, T., Schofield, P. R., and Sprengel, R. (1991). Amino-terminal leucine-rich repeats in gonadotropin receptors determine hormone selectivity. EMBO J. 10, 1885-1890.
10. Brothers, S. P., Cornea, A., Janovick, J. A., and Conn, P. M. (2004). Human loss-of-function gonadotropin-releasing hormone receptor mutants retain wild-type receptors in the endoplasmic reticulum: molecular basis of the dominant-negative effect. Mol. Endocrinol. 18, 1787-1797.
11. Ellgaard, L., and Helenius, A. (2003). Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell. Biol. 4, 181-191.
12. Fabritz, J., Ryan, S., and Ascoli, M. (1998). Transfected cells express mostly the intracellular precursor of the lutropin/choriogonadotropin receptor but this precursor binds choriogonadotropin with high affinity. Biochemistry 37, 664-672.
13. Fan, Q. R., and Hendrickson, W. A. (2005). Structure of human follicle-stimulating hormone in complex with its receptor. Nature 433, 269-277.
14. Frenkel, Z., Shenkman, M., Kondratyev, M., and Lederkremer, G. Z. (2004). Separate roles and different routing of calnexin and ERp57 in endoplasmic reticulum quality control revealed by interactions with asialoglycoprotein receptor chains. Mol. Biol. Cell 15, 2133-2142.
15. Fujiki, Y., Hubbard, A. L., Fowler, S., and Lazarow, P. B. (1982). Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 93, 97-102.
16. Grosse, R., Schöneberg, T., Schultz, G., and Gudermann, T. (1997). Inhibition of gonadotropin-releasing hormone receptor signaling by expression of a splice variant of the human receptor. Mol. Endocrinol. 11, 1305-1318.
17. Guan, X. M., Kobilka, T. S., and Kobilka, B. K. (1992). Enhancement of membrane insertion and function in a type IIIb membrane protein following introduction of a cleavable signal peptide. J. Biol. Chem. 267, 21995-21998.
18. Helenius, A., and Aebi, M. (2004). Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73, 1019-1049.
19. Huppa, J. B., and Ploegh, H. L. (1997). The a chain of the T cell antigen receptor is degraded in the cytosol. Immunity 7, 113-122.
20. Huyer, G., Longsworth, G. L., Mason, D. L., Mallampalli, M. P., McCaffery, J. M., Wright, R. L., and Michaelis, S. (2004). A striking quality control subcompartment in Saccharomyces cerevisiae: the endoplasmic reticulum-associated compartment. Mol. Biol. Cell 15, 908-921.
21. Illing, M. E., Rajan, R. S., Bence, N. F., and Kopito, R. R. (2002). A rhodopsin mutant linked to autosomal dominant retinitis pigmentosa is prone to aggregate and interacts with the ubiquitin proteasome system. J. Biol. Chem. 277, 34150-34160.
22. Imai, Y., Soda, M., Inoue, H., Hattori, N., Mizuno, Y., and Takahashi, R. (2001). An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin. Cell 105, 891-902.
23. Jiang, X., Russo, I. H., and Russo, J. (2002). Alternately spliced luteinizing hormone/human chorionic gonadotropin receptor mRNA in human breast epithelial cells. Int. J. Oncol. 20, 735-738.
24. Johnston, J. A., Ward, C. L., and Kopito, R. R. (1998). Aggresomes: a cellular response to misfolded proteins. J. Cell Biol. 143, 1883-1898.
25. Junn, E., Lee, S. S., Suhr, U. T., and Mouradian, M. M. (2002). Parkin accumulation in aggresomes due to proteasome impairment. J. Biol. Chem. 277, 47870-47877.
26. Kabore, A. F., Wang, W. J., Russo, S. J., and Beers, M. F. (2001). Biosynthesis of surfactant protein C: characterization of aggresome formation by EGFP chimeras containing propeptide mutants lacking conserved cysteine residues. J. Cell Sci. 114, 293-302.
27. Kamhi-Nesher, S., Shenkman, M., Tolchinsky, S., Fromm, S. V., Ehrlich, R., and Lederkremer, G. Z. (2001). A novel quality control compartment derived from the endoplasmic reticulum. Mol. Biol. Cell 12, 1711-1723.
28. Karpa, K. D., Lin, R., Kabbani, N., and Levenson, R. (2000). The dopamine D3 receptor interacts with itself and the truncated D3 splice variant D3nf: D3-D3nf interaction causes mislocalization of D3 receptors. Mol. Pharmacol. 58, 677-683.
29. Kaykas, A., Yang-Snyder, J., Héroux, M., Shah, K. V., Bouvier, M., and Moon, R. T. (2004). Mutant Frizzled 4 associated with vitreoretinopathy traps wild-type Frizzled in the endoplasmic reticulum by oligomerization. Nat. Cell Biol. 6, 52-58.
30. Lakkakorpi, J. T., Pietilä, E. M., Aatsinki, J. T., and Rajaniemi, H. J. (1993). Human chorionic gonadotrophin (CG)-induced down-regulation of the rat luteal LH/CG receptor results in part from the down-regulation of its synthesis, involving increased alternative processing of the primary transcript. J. Mol. Endocrinol. 10, 153-162.
31. Lee, D. H., and Goldberg, A. L. (1998). Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 8, 397-403.
32. Licht, P., von Wolff, M., Berkholz, A., and Wildt, L. (2003). Evidence for cycle-dependent expression of full-length human chorionic gonadotropin/luteinizing hormone receptor mRNA in human endometrium and decidua. Fertil. Steril. 79 (Suppl 1), 718-723.
33. Lin, J., Lei, Z. M., Lojun, S., Rao, C. V., Satyaswaroop, P. G., and Day, T. G. (1994). Increased expression of luteinizing hormone/human chorionic gonadotropin receptor gene in human endometrial carcinomas. J. Clin. Endocrinol. Metab. 79, 1483-1491.
34. Lippincott-Schwartz, J., Yuan, L. C., Bonifacino, J. S., and Klausner, R. D. (1989). Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56, 801-813.
35. Lu, M., Echeverri, F., and Moyer, B. D. (2003). Endoplasmic reticulum retention, degradation, and aggregation of olfactory G-protein coupled receptors. Traffic 4, 416-433.
36. Nakamura, K., Yamashita, S., Omori, Y., and Minegishi, T. (2004). A splice variant of the human luteinizing hormone (LH) receptor modulates the expression of wild-type human LH receptor. Mol. Endocrinol. 18, 1461-1470.
37. Notterpek, L., Ryan, M. C., Tobler, A. R., and Shooter, E. M. (1999). PMP22 accumulation in aggresomes: implications for CMT1A pathology. Neurobiol. Dis. 6, 450-460.
38. Parodi, A. J. (2000). Protein glucosylation and its role in protein folding. Annu. Rev. Biochem. 69, 69-93.
39. Petäjä-Repo, U. E., Hogue, M., Laperrière, A., Bhalla, S., Walker, P., and Bouvier, M. (2001). Newly synthesized human S opioid receptors retained in the endoplasmic reticulum are retrotranslocated to the cytosol, deglycosylated, ubiquitinated, and degraded by the proteasome. J. Biol. Chem. 276, 4416-4423.
40. Petäjä-Repo, U. E., Hogue, M., Laperrière, A., Walker, P., and Bouvier, M. (2000). Export from the endoplasmic reticulum represents the limiting step in the maturation and cell surface expression of the human δ opioid receptor. J. Biol. Chem. 275, 13727-13736.
41. Pierce, J. G., and Parsons, T. F. (1981). Glycoprotein hormones: structure and function. Annu. Rev. Biochem. 50, 465-495.
42. Pietilä, E. M., Tuusa, J. T., Apaja, P. M., Aatsinki, J. T., Hakalahti, A. E., Rajaniemi, H. J., and Petäjä-Repo, U. E. (2005). Inefficient maturation of the rat luteinizing hormone receptor. A putative way to regulate receptor numbers at the cell surface. J. Biol. Chem. 280, 26622-26629.
43. Reinholz, M. M., Zschunke, M. A., and Roche, P. C. (2000). Loss of alternately spliced messenger RNA of the luteinizing hormone receptor and stability of the follicle-stimulating hormone receptor messenger RNA in granulosa cell tumors of the human ovary. Gynecol. Oncol. 79, 264-271.
44. Saliba, R. S., Munro, P. M. G., Luthert, P. J., and Cheetham, M. E. (2002). The cellular fate of mutant rhodopsin: quality control, degradation and aggresome formation. J. Cell Sci. 115, 2907-2918.
45. Sarmiento, J. M., Añazco, C. C., Campos, D. M., Prado, G. N., Navarro, J., and Gonzalez, C. B. (2004). Novel down-regulatory mechanism of the surface expression of the vasopressin V2 receptor by an alternative splice receptor variant. J. Biol. Chem. 279, 47017-47023.
46. Schröder, M., and Kaufman, R. J. (2005). The mammalian unfolded protein response. Annu. Rev. Biochem. 74, 739-789.
47. Slot, J. W., and Geuze, H. J. (1985). A new method of preparing gold probes for multiple-labeling cytochemistry. Eur. J. Cell Biol. 38, 87-93.
48. Sokka, T., Hämäläinen, T., and Huhtaniemi, I. (1992). Functional LH receptor appears in the neonatal rat ovary after changes in the alternative splicing pattern of the LH receptor mRNA. Endocrinology 130, 1738-1740.
49. Steinmeyer, C., Berkholz, A., Gebauer, G., and Jager, W. (2003). The expression of hCG receptor mRNA in four human ovarian cancer cell lines varies considerably under different experimental conditions. Tumour Biol. 24, 13-22.
50. Tena-Sempere, M., Zhang, F. P., and Huhtaniemi, I. (1994). Persistent expression of a truncated form of the luteinizing hormone receptor messenger ribonucleic acid in the rat testis after selective Leydig cell destruction by ethylene dimethane sulfonate. Endocrinology 135, 1018-1024.
51. Tsai-Morris, C. H., Buczko, E., Wang, W., and Dufau, M. L. (1990). Intronic nature of the rat luteinizing hormone receptor gene defines a soluble receptor subspecies with hormone binding activity. J. Biol. Chem. 265, 19385-19388.
52. Vassart, G., Pardo, L., and Costagliola, S. (2004). A molecular dissection of the glycoprotein hormone receptors. Trends Biochem. Sci. 29, 119-126.
53. Wessel, D., and Flugge, U. I. (1984). A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141-143.
54. Wüller, S., Wiesner, B., Löffler, A., Furkert, J., Krause, G., Hermosilla, R., Schaefer, M., Schülein, R., Rosenthal, W., and Oksche, A. (2004). Pharmacochaperones post-translationally enhance cell surface expression by increasing conformational stability of wild-type and mutant vasopressin V2 receptors. J. Biol. Chem. 279, 47254-47263.
55. Xie, Y. B., Wang, H., and Segaloff, D. L. (1990). Extracellular domain of lutropin/choriogonadotropin receptor expressed in transfected cells binds choriogonadotropin with high affinity. J. Biol. Chem. 265, 21411-21414.
56. Yamashita, S., Nakamura, K., Omori, Y., Tsunekawa, K., Murakami, M., and Minegishi, T. (2005). Association of human follitropin (FSH) receptor with splicing variant of human lutropin/choriogonadotropin receptor negatively controls the expression of human FSH receptor. Mol. Endocrinol. 39, 2099-2111.
57. Zhang, F. P., Hämäläinen, T., Kaipia, A., Pakarinen, P., and Huhtaniemi, I. (1994). Ontogeny of luteinizing hormone receptor gene expression in the rat testis. Endocrinology 134, 2206-2213.
58. Zhang, R., Cai, H., Fatima, N., Buczko, E., and Dufau, M. L. (1995). Functional glycosylation sites of the rat luteinizing hormone receptor required for ligand binding. J. Biol. Chem. 270, 21722-21728.