Increased expression of rififylin in a < 330 kb congenic strain is linked to impaired endosomal recycling in proximal tubules

Frontiers in Genetics

Volumn 3, Issue AUG, 2012, Pages

  Gopalakrishnan, Kathirvel ^a   Kumarasamy, Sivarajan ^a   Yan, Yanling ^a,b   Liu, Jiang ^a   Kalinoski, Andrea ^a   Kothandapani, Anbarasi ^a   Farms, Phyllis ^a   Joe, Bina ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b YANSHAN UNIVERSITY   (China)

Author keywords

Carp 2; Gene; Hypertension; Kidney disease; Linkage mapping; Proteinuria; Rat; Rffl

Indexed keywords

CYPRINIDAE; RATTUS;

EID: 84876026563     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2012.00138     Document Type: Article

References (41)

1. Arar, N., Nath, S., Thameem, F., Bauer, R.,Voruganti, S., Comuzzie, A., Cole, S., Blangero, J., MacCluer, J., and Abboud, H. (2007). Genome-wide scans for microalbuminuria in Mexican Americans: the San Antonio Family Heart Study. Genet. Med. 9, 80-87.
2. Arar, N. H., Voruganti, V. S., Nath, S. D., Thameem, F., Bauer, R., Cole, S. A., Blangero, J., MacCluer, J. W., Comuzzie, A. G., and Abboud, H. E. (2008). A genome-wide search for linkage to chronic kidney disease in a community-based sample: the SAFHS. Nephrol. Dial Transplant. 23,3184-3191.
3. Baumert, M., Schlaich, M. P., Nalivaiko, E., Lambert, E., Sari, C. I., Kaye, D. M., Elser, M. D., Sanders, P., and Lambert, G. (2011). Relation between QT interval variability and cardiac sympathetic activity in hypertension. Am. J. Physiol. Heart Circ. Physiol. 300, H1412-H1417.
4. Brown, D., and Stow, J. L. (1996). Protein trafficking and polarity in kidney epithelium: from cell biology to physiology. Physiol Rev. 76, 245-297.
5. Coumailleau, F., Babinet, C., and Cohen-Tannoudji, M. (2005). Inhibition of endocytic recycling by Rififylin. Med. Sci. (Paris) 21,235-237.
6. Coumailleau, F., Das, V., Alcover, A., Raposo, G., Vandormael-Pournin, S., Le Bras, S., Baldacci, P., Dautry-Varsat, A., Babinet, C., and Cohen-Tannoudji, M. (2004). Overexpression of rififylin, a new RING finger and FYVE-like domain-containing protein, inhibits recycling from the endocytic recycling compartment. Mol Biol. Cell 15,4444-4456.
7. Garrett, M. R., Dene, H., and Rapp, J. P. (2003). Time-course genetic analysis of albuminuria in Dahl salt-sensitive rats on low-salt diet. J. Am. Soc. Nephrol. 14, 1175-1187.
8. Garrett, M. R., Gunning, W. T., Radecki, T., and Richard, A. (2007). Dissection of a genetic locus influencing renal function in the rat and its concordance with kidney disease loci on human chromosome 1q21. Physiol. Genomics 30, 322-334.
9. Garrett, M. R., Pezzolesi, M. G., and Korstanje, R. (2010). Integrating human and rodent data to identify the genetic factors involved in chronic kidney disease. J. Am. Soc. Nephrol. 21,398-405.
10. Golachowska, M. R., Hoekstra, D., and van Ijzendoorn, S. C. (2010). Recycling endosomes in apical plasma membrane domain formation and epithelial cell polarity. Trends Cell Biol. 20,618-626.
11. Gopalakrishnan, K., Morgan, E. E., Yerga-Woolwine, S., Farms, P., Kumarasamy, S., Kalinoski, A., Liu, X.,Wu,J.,Liu,L., and Joe, B. (2011). Augmented rififylin is a risk factor linked to aberrant cardiomyocyte function, short-QT interval and hypertension. Hypertension 57, 764-771.
12. Grant, B. D., and Donaldson, J. G. (2009). Pathways and mechanisms of endocytic recycling. Nat. Rev. Mol. Cell Biol. 10, 597-608.
13. Hryciw, D. H., Ekberg, J., Pollock, C. A., and Poronnik, P. (2006). ClC-5: a chloride channel with multiple roles in renal tubular albumin uptake. Int. J. Biochem. Cell Biol. 38, 1036-1042.
14. Hwang, S. J., Yang, Q., Meigs, J. B., Pearce, E. N., and Fox, C. S. (2007). A genome-wide association for kidney function and endocrine-related traits in the NHLBI's Framing-ham Heart Study. BMCMed. Genet. 8(Suppl. 1), S10. doi:10.1186/1471-2350-8-S1-S10
15. Iyengar, S. K., Abboud, H. E., Goddard, K. A., Saad, M. F., Adler, S. G., Arar, N. H., Bowden, D. W., Duggirala, R., Elston, R. C., Hanson, R. L., Ipp, E., Kao, W. H., Kimmel, P. L., Klag, M. J., Knowler, W. C., Meoni, L. A., Nelson, R. G., Nicholas, S. B., Pahl, M. V., Parekh, R. S., Quade, S. R., Rich, S. S., Rotter, J. I., Scavini, M., Schelling, J. R., Sedor, J. R., Sehgal, A. R., Shah, V. O., Smith, M. W., Taylor, K. D., Winkler, C. A., Zager, P. G., and Freedman, B. I. (2007). Genome-wide scans for diabetic nephropathy and albuminuria in multiethnic populations: the family investigation of nephropathy and diabetes (FIND). Diabetes 56, 1577-1585.
16. Krolewski, A. S., Poznik, G. D., Placha, G., Canani, L., Dunn, J., Walker, W., Smiles, A., Krolewski, B., Fogarty, D. G., Moczulski, D., Araki, S., Makita, Y., Ng, D. P., Rogus, J., Duggirala, R., Rich, S. S., and Warram, J. H. (2006). A genome-wide linkage scan for genes controlling variation in urinary albumin excretion in type II diabetes. Kidney Int. 69, 129-136.
17. Kumarasamy, S., Gopalakrishnan, K., Toland, E. J., Yerga-Woolwine, S., Farms, P., Morgan, E. E., and Joe, B. (2011). Refined mapping of blood pressure quantitative trait loci using congenic strains developed from two genetically hypertensive rat models. Hypertens. Res. 34, 1263-1270.
18. Leon, J. M., Freedman, B. I., Miller, M. B., North, K. E., Hunt, S. C., Eckfeldt, J. H., Lewis, C. E., Kraja, A. T., Djousse, L., and Arnett, D. K. (2007). Genome scan of glomerular filtration rate and albuminuria: the HyperGEN study. Nephrol Dial. Transplant. 22, 763-771.
19. Liu, J., Kesiry, R., Periyasamy, S. M., Malhotra, D., Xie, Z., and Shapiro, J. I. (2004). Ouabain induces endocytosis of plasmalemmal Na/K-ATPase in LLC-PK1 cells by a clathrin-dependent mechanism. Kidney Int. 66,227-241.
20. Liu, J., Periyasamy, S. M., Gunning, W., Fedorova, O. V., Bagrov, A. Y., Malhotra, D., Xie, Z., and Shapiro, J. I. (2002). Effects of cardiac glycosides on sodium pump expression and function in LLC-PK1 and MDCK cells. Kidney Int. 62, 2118-2125.
21. Liu, J., Yan, Y., Liu, L., Xie, Z., Malhotra, D., Joe, B., and Shapiro, J. I. (2011). Impairment of Na/K-ATPase signaling in renal proximal tubule contributes to Dahl salt-sensitive hypertension. J. Biol Chem. 286, 22806-22813.
22. Liu, Y., and Freedman, B. I. (2005). Genetics of progressive renal failure in diabetic kidney disease. Kidney Int.Suppl. 99,S94-S97.
23. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408.
24. Marshansky, V., Ausiello, D. A., and Brown, D. (2002). Physiological importance of endosomal acidification: potential role in proximal tubulopathies. Curr. Opin. Nephrol. Hypertens. 11,527-537.
25. Martinez, F., Mansego, M. L., Chaves, E J., and Redon, J. (2010). Genetic bases of urinary albumin excretion and related traits in hypertension. J. Hypertens. 28,213-225.
26. Maxfield, F. R., and McGraw, T. E. (2004). Endocytic recycling. Nat. Rev. Mol Cell Biol. 5, 121-132.
27. Meyer-Schwesinger, C., Meyer, T. N., Sievert, H., Hoxha, E., Sachs, M., Klupp, E. M., Munster, S., Balabanov, S., Carrier, L., Helmchen, U., Thaiss, E, and Stahl, R. A. (2011). Ubiquitin C-terminal hydrolasel1 activity induces polyubiquitin accumulation in podocytes and increases protein-uria in rat membranous nephropathy. Am. J. Pathol. 178, 2044-2057.
28. Newton-Cheh, C., Eijgelsheim, M., Rice, K. M., de Bakker, P. I., Yin, X., Estrada, K., Bis, J. C., Marciante, K., Rivadeneira, F., Noseworthy, P. A., Sotoodehnia, N., Smith, N. L., Rotter, J. I., Kors, J. A., Witteman, J. C., Hofman, A., Heckbert, S. R., O'Donnell, C. J., Uitterlinden, A. G., Psaty, B. M., Lumley, T., Larson, M. G., and Stricker, B. H. (2009). Common variants at ten loci influence QT interval duration in the QTGEN Study. Nat. Genet. 41, 399-406.
29. Nielsen, R., and Christensen, E. I. (2010). Proteinuria and events beyond the slit. Pediatr. Nephrol. 25, 813-822.
30. Nielsen, S. (1993). Endocytosis in proximal tubule cells involves a two-phase membrane-recyclingpathway. Am. J. Physiol. 264, C823-C835.
31. Nielsen, S. (1994). Endocytosis in renal proximal tubules. Experimental electron microscopical studies of protein absorption and membrane traffic in isolated, in vitro perfused proximal tubules. Dan. Med. Bull. 41,243-263.
32. Pfeufer, A., Sanna, S., Arking, D. E., Muller, M., Gateva, V., Fuchsberger, C., Ehret, G. B., Orru, M., Pattaro, C., Kottgen, A., Perz, S., Usala, G., Barbalic, M., Li, M., Putz, B., Scuteri, A., Prineas, R. J., Sinner, M. F., Gieger, C., Najjar, S. S., Kao, W. H., Muhleisen, T. W., Dei, M., Happle, C., Mohlenkamp, S., Crisponi, L., Erbel, R., Jockel, K. H., Naitza, S., Steinbeck, G., Marroni, F., Hicks, A. A., Lakatta, E., Muller-Myhsok, B., Pramstaller, P. P., Wichmann, H. E., Schlessinger, D., Boerwinkle, E., Meitinger, T., Uda, M., Coresh, J., Kaab, S., Abecasis, G.R.,and Chakravarti,A. (2009). Common variants at ten loci modulate the QT interval duration in the QTSCD Study. Nat. Genet. 41, 407-414.
33. Schweitzer, J. K., Sedgwick, A. E., and D'Souza-Schorey, C. (2011). ARF6-mediated endocytic recycling impacts cell movement, cell division and lipid homeostasis. Semin. Cell Dev. Biol. 22, 39-47.
34. Steinman, R. M., Mellman, I. S., Muller, W.A.,and Cohn,Z.A. (1983).Endocytosis and the recycling of plasma membrane. J. Cell Biol. 96,1-27.
35. Stendel, C., Roos, A., Kleine,H., Arnaud, E., Ozcelik, M., Sidiropoulos, P. N., Zenker, J., Schupfer, F., Lehmann, U., Sobota, R. M., Litchfield, D. W., Luscher, B., Chrast, R., Suter, U., and Senderek, J. (2010). SH3TC2, a protein mutant in Charcot-Marie-Tooth neuropathy, links peripheral nerve myelination to endosomal recycling. Brain 133, 2462-2474.
36. Sterken, R., and Kiryluk, K. (2010). The genetics of albuminuria: from haplotype association mapping in mice to genetic causation in humans. Kidney Int. 77, 173-175.
37. Sterzel, R. B., Luft, E C., Gao, Y., Schnermann, J., Briggs, J. P., Ganten, D., Waldherr, R., Schnabel, E., and Kriz, W. (1988). Renal disease and the development of hypertension in salt-sensitive Dahl rats. Kidney Int. 33, 1119-1129.
38. Sustarsic, D. L., McPartland, R. P., and Rapp, J. P. (1981). Developmental patterns of blood pressure and urinary protein, kallikrein, and prostaglandin E2 in Dahl salt-hypertension-susceptible rats. J. Lab. Clin. Med. 98, 599-606.
39. Trischler, M., Stoorvogel, W., and Ullrich, O. (1999). Biochemical analysis of distinct Rab5- and Rab 11-positive endosomes along the transferrin pathway.J. CellSci. 112,4773-4783.
40. Turner, S. T., Kardia, S. L., Mosley, T. H., Rule, A. D., Boerwinkle, E., and de Andrade, M. (2006). Influence of genomic loci on measures of chronic kidney disease in hypertensive sibships. J. Am. Soc. Nephrol. 17, 2048-2055.
41. Yamamoto, K., Cox, J. P., Friedrich, T., Christie, P. T., Bald, M., Houtman, P. N., Lapsley, M. J., Patzer, L., Tsimaratos, M., Van, T. H. W. G., Yamaoka, K., Jentsch, T. J., and Thakker, R. V. (2000). Characterization of renal chloride channel (CLCN5) mutations in Dent's disease. J. Am. Soc. Nephrol. 11, 1460-1468.