Luteinizing Hormone Receptors are Confined in Mesoscale Plasma Membrane Microdomains Throughout Recovery from Receptor Desensitization

Cell Biochemistry and Biophysics

Volumn 68, Issue 3, 2014, Pages 561-569

  Wolf Ringwall, Amber L ^a   Winter, Peter W ^a   Roess, Deborah A ^a   George Barisas, B ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Human chorionic gonadotropin; Lateral diffusion; Luteinizing hormone receptor; Plasma membrane microdomains; Receptor desensitization; Single particle tracking

Indexed keywords

CRICETULUS GRISEUS;

CHORIONIC GONADOTROPIN; LUTEINIZING HORMONE; LUTEINIZING HORMONE RECEPTOR;

ANIMAL; ARTICLE; CELL MEMBRANE; CHO CELL LINE; CRICETULUS; DRUG EFFECT; HAMSTER; HUMAN; METABOLISM; PROTEIN TRANSPORT;

ANIMALS; CHO CELLS; CHORIONIC GONADOTROPIN; CRICETINAE; CRICETULUS; HUMANS; LUTEINIZING HORMONE; MEMBRANE MICRODOMAINS; PROTEIN TRANSPORT; RECEPTORS, LH;

EID: 84896031137     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12013-013-9738-x     Document Type: Article

References (35)

1. 2-Adrenergic receptor signaling and desensitization elucidated by quantitative modeling of real time cAMP dynamics. Journal of Biological Chemistry, 283, 2949-2961.
2. Downs, S. M., & Hunzicker-Dunn, M. (1995). Differential regulation of oocyte maturation and cumulus expansion in the mouse oocyte-cumulus cell complex by site-selective analogs of cyclic adenosine monophosphate. Developmental Biology, 172, 72-85.
3. Smith, S. M., Lei, Y., Liu, J., Cahill, M. E., Hagen, G. M., Barisas, B. G., et al. (2006). Luteinizing hormone receptors translocate to plasma membrane microdomains after binding of human chorionic gonadotropin. Endocrinology, 147, 1789-1795.
4. Wolf-Ringwall, A. L., Winter, P. W., Liu, J., van Orden, A. K., Roess, D. A., & Barisas, B. G. (2011). Restricted lateral diffusion of luteinizing hormone receptors in membrane microdomains. Journal of Biological Chemistry, 286, 29818-29827.
5. Claing, A., Laporte, S. A., Caron, M. G., & Lefkowitz, R. J. (2002). Endocytosis of G protein-coupled receptors: Roles of G protein-coupled receptor kinases and β-arrestin proteins. Progress in Neurobiology, 66, 61-79.
6. Horvat, R. D., Barisas, B. G., & Roess, D. A. (2001). Luteinizing hormone receptors are self-associated in slowly diffusing complexes during receptor desensitization. Molecular Endocrinology, 15, 534-542.
7. Dix, C. J., Schumacher, M., & Cooke, B. A. (1982). Desensitization of tumor Leydig cells by lutropin: Evidence for uncoupling of the lutropin receptor from the guanine nucleotide-binding protein. Biochemistry Journal, 202, 739-745.
8. Lamm, M. L. G., & Hunzicker-Dunn, M. (1994). Phosphorylation-independent desensitzation of the luteinizing hormone/chorionic gonadotropin receptor in porcine follicular membranes. Molecular Endocrinology, 8(11), 1537-1546.
9. Roess, D. A., Niswender, G. D., & Barisas, B. G. (1988). Cytochalasins and colchicine increase the lateral mobility of human chorionic gonadotropin-occupied luteinizing hormone receptors on ovine luteal cells. Endocrinology, 122, 261-269.
10. Kusumi, A., Shirai, Y. M., Koyama-Honda, I., Suzuki, K. G. N., & Fujiwara, T. K. (2010). Hierarchical organization of the plasma membrane: Investigations by single-molecule tracking vs. fluorescence correlation spectroscopy. FEBS Letters, 584, 1814-1823.
11. Jacobson, K., Mouritsen, O. G., & Anderson, R. G. (2007). Lipid rafts: At a crossroad between cell biology and physics. Nature Cell Biology, 9, 7-14.
12. Pike, L. J. (2006). Rafts defined: A report on the Keystone symposium on lipid rafts and cell function. Journal of Lipid Research, 47, 1597-1598.
13. Lajoie, P., Goetz, J. G., Dennis, J. W., & Nabi, I. R. (2009). Lattices, rafts, and scaffolds: Domain regulation of receptor signaling at the plasma membrane. The Journal of Cell Biology, 185, 381-385.
14. Simons, K., & Toomre, D. (2000). Lipid rafts and signal transduction. Nature Reviews Molecular Cell Biology, 1, 31-39.
15. Hunzicker-Dunn, M., Barisas, B. G., Song, J., & Roess, D. A. (2003). Membrane organization of luteinizing hormone receptors differs between actively signaling and desensitized receptors. Journal of Biological Chemistry, 278, 42744-42749.
16. Amsterdam, A., Berkowitz, A., Nimrod, A., & Kohen, F. (1980). Aggregation of luteinizing hormone receptors in granulosa cells: A possible mechanism for desensitization to the hormone. Proceedings of the National Academy of Sciences USA, 77, 3440-3445.
17. Sanchez-Yague, J., Rodriquez, M. C., Segaloff, D. L., & Ascoli, M. (1992). Truncation of the cytoplasmic tail of the lutropin/choriogonadotropin receptor prevents agonist-induced uncoupling. Journal of Biological Chemistry, 267, 7217-7220.
18. Roess, D. A., Smith, S. M. L., Winter, P., Zhou, J., Dou, P., Baruah, B., et al. (2008). Effects of vanadium-containing compounds on membrane lipids and on microdomains used in receptor-mediated signaling. Chemistry & Biodiversity, 5, 1558-1570.
19. Winter, P. W., Al-Qatati, A., Wolf-Ringwall, A. L., Schoeberl, S., Chatterjee, P. B., Barisas, B. G., et al. (2012). The anti-diabetic bis(maltolato)oxovanadium(iv) decreases lipid order while increasing insulin receptor localization in membrane microdomains. Dalton Transactions, 41, 6419-6430.
20. Kusumi, A., Sako, Y., & Yamamoto, M. (1993). Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophysical Journal, 65, 2021-2040.
21. Barisas, B. G., Smith, S. M., Liu, J., Song, J., Hagen, G. M., Pecht, I., et al. (2007). Compartmentalization of the Type I Fc epsilon receptor and MAFA on mast cell membranes. Biophysical Chemistry, 126, 209-217.
22. Saxton, M. J. (1997). Single-particle tracking: The distribution of diffusion coefficients. Biophysical Journal, 72, 1744-1753.
23. Lei, Y., Hagen, G. M., Smith, S. M., Liu, J., Barisas, G., Roess, D. A., et al. (2007). Constitutively-active human LH receptors are self-associated and located in rafts. Molecular and Cellular Endocrinology, 260-262, 65-72.
24. Lefkowitz, R. (1998). G protein-coupled receptors. The Journal of Biological Chemistry, 273, 18677-18680.
25. Horvat, R. D., Nelson, S., Clay, C. M., Barisas, B. G., & Roess, D. A. (1999). Intrinsically fluorescent luteinizing hormone receptor demonstrates hormone-driven aggregation. Biochemical and Biophysical Research Communications, 255, 382-385.
26. 2α and ferritin-LH. Endocrinology, 115, 2217-2225.
27. Linderman, J. J. (2009). Modeling of G-protein-coupled receptor signaling pathways. Journal of Biological Chemistry, 284, 5427-5431.
28. Francis, S. H., Blount, M. A., & Corbin, J. D. (2011). Mammalian cyclic nucleotide phosphodiesterases: Molecular mechanisms and physiological functions. Physiological Reviews, 91, 651-690.
29. Hunzicker-Dunn, M., Barisas, G., Song, J., & Roess, D. A. (2003). Membrane organization of luteinizing hormone receptors differs between actively signaling and desensitized receptors. Journal of Biological Chemistry, 278, 42744-42749.
30. Niswender, G. D., Roess, D. A., Sawyer, H. R., Silvia, W. J., & Barisas, B. G. (1985). Differences in the lateral mobility of receptors for luteinizing hormone (LH) in the luteal cell plasma membrane when occupied by ovine LH versus human chorionic gonadotropin. Endocrinology, 116, 164-169.
31. Dragsten, P., Henkart, P., Blumenthal, R., Weinstein, J., & Schlessinger, J. (1979). Lateral diffusion of surface immunoglobulin, Thy-1 antigen, and a lipid probe in lymphocyte plasma membranes. Proceedings of the National Academy of Science USA, 76, 5163-5167.
32. Godin, A. G., Costantino, S., Lorenzo, L.-E., Swift, J. L., Sergeev, M., Ribeiro-da-Silva, A., et al. (2011). Revealing protein oligomerization and densities in situ using spatial intensity distribution analysis. Proceedings of the National Academy of Sciences USA, 108, 7010-7015.
33. Saffarian, S., Li, U., Elson, E., & Pike, L. (2007). Oligomerization of the EGF receptor investigated by life cell fluorescence intensity distribution analysis. Biophysical Journal, 93, 1021-1031.
34. Roess, D. A., Brady, C. J., & Barisas, B. G. (2000). Biological function of the LH receptor is associated with slow receptor rotational diffusion. Biochimica et Biophysica Acta, 1464, 242-250.
35. Liu, Z., Rudd, M. D., Hernandez-Gonzalez, I., Gonzalez-Robayna, I., Fan, H.-Y., Zeleznik, A. J., et al. (2009). FSH and FOXO1 Regulate genes in the sterol/steroid and lipid biosynthetic pathways in granulosa cells. Molecular Endocrinology, 23, 649-661.