ATP-2 Interacts with the PLAT Domain of LOV-1 and Is Involved inCaenorhabditis elegansPolycystin Signaling

Molecular Biology of the Cell - Tập 16 Số 2 - Trang 458-469 - 2005
Jinghua Hu1, Maureen M. Barr1
1Division of Pharmaceutical Sciences, School of Pharmacy, University of Wisconsin-Madison, Madison, WI 53705

Tóm tắt

Caenorhabditis elegans is a powerful model to study the molecular basis of autosomal dominant polycystic kidney disease (ADPKD). ADPKD is caused by mutations in the polycystic kidney disease (PKD)1 or PKD2 gene, encoding polycystin (PC)-1 or PC-2, respectively. The C. elegans polycystins LOV-1 and PKD-2 are required for male mating behaviors and are localized to sensory cilia. The function of the evolutionarily conserved polycystin/lipoxygenase/α-toxin (PLAT) domain found in all PC-1 family members remains an enigma. Here, we report that ATP-2, the β subunit of the ATP synthase, physically associates with the LOV-1 PLAT domain and that this interaction is evolutionarily conserved. In addition to the expected mitochondria localization, ATP-2 and other ATP synthase components colocalize with LOV-1 and PKD-2 in cilia. Disrupting the function of the ATP synthase or overexpression of atp-2 results in a male mating behavior defect. We further show that atp-2, lov-1, and pkd-2 act in the same molecular pathway. We propose that the ciliary localized ATP synthase may play a previously unsuspected role in polycystin signaling.

Từ khóa


Tài liệu tham khảo

Aguiari, G.et al.(2004). Deficiency of polycystin-2 reduces Ca2+ channel activity and cell proliferation in ADPKD lymphoblastoid cells.FASEB J.18, 884-886.

Arakaki, N., Nagao, T., Niki, R., Toyofuku, A., Tanaka, H., Kuramoto, Y., Emoto, Y., Shibata, H., Magota, K., and Higuti, T. (2003). Possible role of cell surface H(+)-ATP synthase in the extracellular ATP synthesis and proliferation of human umbilical vein endothelial cells.Mol. Cancer Res.1, 931-939.

Bae, T. J.et al.(2004). Lipid raft proteome reveals ATP synthase complex in the cell surface.Proteomics.4, 3536-3548.

Bakhtiari, N., Lai-Zhang, J., Yao, B., and Mueller, D. M. (1999). Structure/function of the beta-barrel domain of F1-ATPase in the yeastSaccharomyces cerevisiae. J. Biol.Chem.274, 16363-16369.

Bargmann, C. I., Hartwieg, E., and Horvitz, H. R. (1993). Odorant-selective genes and neurons mediate olfaction inC. elegans.Cell74, 515-527.

Barr, M. M., DeModena, J., Braun, D., Nguyen, C. Q., Hall, D. H., and Sternberg, P. W. (2001). TheCaenorhabditis elegansautosomal dominant polycystic kidney disease gene homologslov-1andpkd-2act in the same pathway.Curr. Biol.11, 1341-1346.

Barr, M. M., and Sternberg, P. W. (1999). A polycystic kidney-disease gene homologue required for male mating behaviour inC. elegans.Nature401, 386-389.

Bateman, A., and Sandford, R. (1999). The PLAT domain: a new piece in the PKD1 puzzle.Curr. Biol.9, R588-R590.

Boletta, A., and Germino, G. G. (2003). Role of polycystins in renal tubulogenesis.Trends Cell Biol.13, 484-492.

Boyer, P. D. (1997). The ATP synthase-a splendid molecular machine.Annu. Rev. Biochem.66, 717-749.

Brenner, S. (1974). The genetics ofCaenorhabditis elegans.Genetics77, 71-94.

Burwick, N. R., Wahl, M. L., Fang, J., Zhong, Z., Capaldi, R. A., Kenan, D. J., and Pizzo, S. V. (2004). An inhibitor of the F1 subunit of ATP synthase (IF1) modulates the activity of angiostatin on the endothelial cell surface.J. Biol. Chem.(in press).

Chang, S. Y., Park, S. G., Kim, S., and Kang, C. Y. (2002). Interaction of the C-terminal domain of p43 and the alpha subunit of ATP synthase.Its functional implication in endothelial cell proliferation. J. Biol. Chem.277, 8388-8394.

Das, B., Mondragon, M. O., Sadeghian, M., Hatcher, V. B., and Norin, A. J. (1994). A novel ligand in lymphocyte-mediated cytotoxicity: expression of the beta subunit of H+ transporting ATP synthase on the surface of tumor cell lines.J. Exp. Med.180, 273-281.

Fraser, A. G., Kamath, R. S., Zipperlen, P., Martinez-Campos, M., Sohrmann, M., and Ahringer, J. (2000). Functional genomic analysis ofC. eleganschromosome I by systematic RNA interference.Nature408, 325-330.

Geng, L.et al.(1996). Identification and localization of polycystin, the PKD1 gene product.J. Clin. Investig.98, 2674-2682.

Gonczy, P.et al.(2000). Functional genomic analysis of cell division inC. elegansusing RNAi of genes on chromosome III.Nature408, 331-336.

Granato, M., Schnabel, H., and Schnabel, R. (1994).pha-1, a selectable marker for gene transfer inC. elegans.Nucleic Acids Res.22, 1762-1763.

Hanazawa, M., Mochii, M., Ueno, N., Kohara, Y., and Iino, Y. (2001). Use of cDNA subtraction and RNA interference screens in combination reveals genes required for germ-line development inCaenorhabditis elegans.Proc. Natl. Acad. Sci. USA98, 8686-8691.

Hodgkin, J. (1983). Male phenotypes and mating efficiency inCaenorhabditis elegans.Geneitcs103, 43-64.

Hooper, K. M., Unwin, R. J., and Sutters, M. (2003). The isolated C-terminus of polycystin-1 promotes increased ATP-stimulated chloride secretion in a collecting duct cell line.Clin. Sci.104, 217-221.

Ibraghimov-Beskrovnaya, O.et al.(1997). Polycystin: in vitro synthesis, in vivo tissue expression, and subcellular localization identifies a large membrane-associated protein.Proc. Natl. Acad. Sci. USA94, 6397-6402.

Igarashi, P., and Somlo, S. (2002). Genetics and pathogenesis of polycystic kidney disease.J. Am. Soc. Nephrol.13, 2384-2398.

Kamath, R. S.et al.(2003). Systematic functional analysis of theCaenorhabditis elegansgenome using RNAi.Nature421, 231-237.

Kamath, R. S., Martinez-Campos, M., Zipperlen, P., Fraser, A. G., and Ahringer, J. (2001). Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA inCaenorhabditis elegans.Genome Biol.2, 1-10.

Kloda, A., Clements, J. D., Lewis, R. J., and Adams, D. J. (2004). Adenosine triphosphate acts as both a competitive antagonist and a positive allosteric modulator at recombinant N-methyl-D-aspartate receptors.Mol. Pharmacol.65, 1386-1396.

Koushika, S. P., and Nonet, M. L. (2000). Sorting and transport inC. elegans: a model system with a sequenced genome.Curr. Opin. Cell Biol.12, 517-523.

Leipziger, J. (2003). Control of epithelial transport via luminal P2 receptors.Am. J. Physiol.284, F419-F432.

Li, N., Shaw, A. R., Zhang, N., Mak, A., and Li, L. (2004). Lipid raft proteomics: analysis of in-solution digest of sodium dodecyl sulfate-solubilized lipid raft proteins by liquid chromatography-matrix-assisted laser desorption/ionization tandem mass spectrometry.Proteomics4, 3156-3166.

Liu, K. S., and Sternberg, P. W. (1995). Sensory regulation of male mating behavior inCaenorhabditis elegans.Neuron14, 79-89.

Martinez, L. O.et al.(2003). Ectopic beta-chain of ATP synthase is an apolipoprotein A-I receptor in hepatic HDL endocytosis.Nature421, 75-79.

Mello, C., and Fire, A. (1995). DNA transformation.Methods Cell Biol.48, 451-482.

Moser, T. L., Kenan, D. J., Ashley, T. A., Roy, J. A., Goodman, M. D., Misra, U. K., Cheek, D. J., and Pizzo, S. V. (2001). Endothelial cell surface F1-F0 ATP synthase is active in ATP synthesis and is inhibited by angiostatin.Proc. Natl. Acad. Sci. USA98, 6656-6661.

Moser, T. L., Stack, M. S., Asplin, I., Enghild, J. J., Hojrup, P., Everitt, L., Hubchak, S., Schnaper, H. W., and Pizzo, S. V. (1999). Angiostatin binds ATP synthase on the surface of human endothelial cells.Proc. Natl. Acad. Sci. USA96, 2811-2816.

Pazour, G. J., San Agustin, J. T., Follit, J. A., Rosenbaum, J. L., and Witman, G. B. (2002). Polycystin-2 localizes to kidney cilia and the ciliary level is elevated inorpkmice with polycystic kidney disease.Curr. Biol.12, R378-R380.

Penefsky, H. S., and Cross, R. L. (1991). Structure and mechanism of FoF1-type ATP synthases and ATPases.Adv. Enzymol. Relat. Areas Mol. Biol.64, 173-214.

Piano, F., Schetter, A. J., Morton, D. G., Gunsalus, K. C., Reinke, V., Kim, S. K., and Kemphues, K. J. (2002). Gene clustering based on RNAi phenotypes of ovary-enriched genes inC. elegans.Curr. Biol.12, 1959-1964.

Rosenbaum, J. L., and Witman, G. B. (2002). Intraflagellar transport.Nat. Rev. Mol. Cell. Biol.3, 813-825.

Schwiebert, E. M.et al.(2002). Autocrine extracellular purinergic signaling in epithelial cells derived from polycystic kidneys.Am. J. Physiol.282, F763-F775.

Schwiebert, E. M., and Zsembery, A. (2003). Extracellular ATP as a signaling molecule for epithelial cells.Biochim. Biophys. Acta1615, 7-32.

Sengupta, P., Chou, J. H., and Bargmann, C. I. (1996).odr-10encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl.Cell84, 899-909.

Simmer, F., Moorman, C., Van Der Linden, A. M., Kuijk, E., Van Den Berghe, P. V., Kamath, R., Fraser, A. G., Ahringer, J., and Plasterk, R. H. (2003). Genome-Wide RNAi ofC. elegansusing the hypersensitiverrf-3strain reveals novel gene functions.PLoS Biol.1, E12.

Simmer, F., Tijsterman, M., Parrish, S., Koushika, S. P., Nonet, M. L., Fire, A., Ahringer, J., and Plasterk, R. H. (2002). Loss of the putative RNA-directed RNA polymerase RRF-3 makesC. eleganshypersensitive to RNAi.Curr. Biol.12, 1317-1319.

Sulston, J. E., Albertson, D. G., and Thomson, J. N. (1980). TheCaenorhabditis elegansmale: postembryonic development of nongonadal structures.Dev. Biol.78, 542-576.

Tavernarakis, N., Wang, S. L., Dorovkov, M., Ryazanov, A., and Driscoll, M. (2000). Heritable and inducible genetic interference by double-stranded RNA encoded by transgenes.Nat. Genet.24, 180-183.

Timmons, L., Court, D. L., and Fire, A. (2001). Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference inCaenorhabditis elegans.Gene263, 103-112.

Tsang, W. Y., and Lemire, B. D. (2002). Mitochondrial genome content is regulated during nematode development.Biochem. Biophys. Res. Commun.291, 8-16.

Tsang, W. Y., Sayles, L. C., Grad, L. I., Pilgrim, D. B., and Lemire, B. D. (2001). Mitochondrial respiratory chain deficiency inCaenorhabditis elegansresults in developmental arrest and increased life span.J. Biol. Chem.276, 32240-32246.

Watnick, T., and Germino, G. (2003). From cilia to cyst.Nat. Genet.34, 355-356.

White, J. G., Southgate, E., Thomson, J. N., and Brenner, S. (1986). The structure of the nervous system of the nematodeCaenorhabditis elegans: the mind of a worm.Phil. Trans. R. Soc. Lond.314, 1-340.

Wildman, S. S., Hooper, K. M., Turner, C. M., Sham, J. S., Lakatta, E. G., King, B. F., Unwin, R. J., and Sutters, M. (2003). The isolated cytoplasmic C-terminus of polycystin-1 prolongs ATP-stimulated chloride conductance through increased agonist stimulated calcium entry.Renal Physiol.285, 1168-1178.

Wilson, P. D., Hovater, J. S., Casey, C. C., Fortenberry, J. A., and Schwiebert, E. M. (1999). ATP release mechanisms in primary cultures of epithelia derived from the cysts of polycystic kidneys.J. Am. Soc. Nephrol.10, 218-229.

Yoder, B. K., Hou, X., and Guay-Woodford, L. M. (2002). The polycystic kidney disease proteins, polycystin-1, polycystin-2, polaris, and cystin, are co-localized in renal cilia.J. Am. Soc. Nephrol.13, 2508-2516.