Rab38 modulates proteinuria in model of hypertension-associated renal disease

Journal of the American Society of Nephrology

Volumn 24, Issue 2, 2013, Pages 283-292

  Rangel Filho, Artur ^a   Lazar, Jozef ^a   Moreno, Carol ^a   Geurts, Aron ^a   Jacob, Howard J ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; COLLOIDAL GOLD; MESSENGER RNA; PROTEIN RAB38; RAB PROTEIN; UNCLASSIFIED DRUG;

ALBUMINURIA; ALLELE; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; FAWN HOODED HYPERTENSIVE RAT; GENE SILENCING; GLOMERULUS FILTRATION; HYPERTENSION; KIDNEY DISEASE; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; LLC PK1 CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN URINE LEVEL; PROTEINURIA; RAT; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY;

EID: 84873357210     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2012090927     Document Type: Article

References (52)

1. McCarthy MI, Hirschhorn JN: Genome-wide association studies: Potential next steps on a genetic journey. Hum Mol Genet 17[R2]:R156-R165, 2008
2. Lander ES, Schork NJ: Genetic dissection of complex traits. Science 265:2037-2048, 1994
3. Schork NJ: Genetics of complex disease: Approaches, problems, and solutions. Am J Respir Crit Care Med 156:S103-S109, 1997
4. Pattaro C, Köttgen A, Teumer A, Garnaas M, Böger CA, Fuchsberger C, Olden M, Chen M-H, Tin A, Taliun D, Li M, Gao X, Gorski M, Yang Q, Hundertmark C, Foster MC, O'Seaghdha CM, Glazer N, Isaacs A, Liu C-T, Smith AV, O'Connell JR, Struchalin M, Tanaka T, Li G, Johnson AD, Gierman HJ, Feitosa M, Hwang S-J, Atkinson EJ, Lohman K, Cornelis MC, Johansson Å, Tönjes A, Dehghan A, Chouraki V, Holliday EG, Sorice R, Kutalik Z, Lehtimäki T, Esko T, Deshmukh H, Ulivi S, Chu AY, Murgia F, Trompet S, Imboden M, Kollerits B, Pistis G, Harris TB, Launer LJ, Aspelund T, Eiriksdottir G, Mitchell BD, Boerwinkle E, Schmidt H, Cavalieri M, Rao M, Hu FB, Demirkan A, Oostra BA, de Andrade M, Turner ST, Ding J, Andrews JS, Freedman BI, Koenig W, Illig T, Döring A, Wichmann H-E, Kolcic I, Zemunik T, Boban M, Minelli C, Wheeler HE, Igl W, Zaboli G, Wild SH, Wright AF, Campbell H, Ellinghaus D, Nöthlings U, Jacobs G, Biffar R, Endlich K, Ernst F, Homuth G, Kroemer HK, Nauck M, Stracke S, Völker U, Völzke H, Kovacs P, Stumvoll M, Mägi R, Hofman A, Uitterlinden AG, Rivadeneira F, Aulchenko YS, Polasek O, Hastie N, Vitart V, Helmer C, Wang JJ, Ruggiero D, Bergmann S, Kähönen M, Viikari J, Nikopensius T, Province M, Ketkar S, Colhoun H, Doney A, Robino A, Giulianini F, Krämer BK, Portas L, Ford I, Buckley BM, Adam M, Thun G-A, Paulweber B, Haun M, Sala C, Metzger M, Mitchell P, Ciullo M, Kim SK, Vollenweider P, Raitakari O, Metspalu A, Palmer C, Gasparini P, Pirastu M, Jukema JW, Probst-Hensch NM, Kronenberg F, Toniolo D, Gudnason V, Shuldiner AR, Coresh J, Schmidt R, Ferrucci L, Siscovick DS, van Duijn CM, Borecki I, Kardia S L R, Liu Y, Curhan GC, Rudan I, Gyllensten U, Wilson JF, Franke A, Pramstaller PP, Rettig R, Prokopenko I, Witteman J C M, Hayward C, Ridker P, Parsa A, Bochud M, Heid IM, Goessling W, Chasman DI, Kao W H L, Fox CS; CARDIo-GRAM ConsortiumICBP ConsortiumCARe ConsortiumWellcome Trust Case Control Consortium 2 (WTCCC2): Genome-wide association and functional follow-up reveals new loci for kidney function. PLoS Genet 8:e1002584, 2012
5. Adeyemo A, Gerry N, Chen G, Herbert A, Doumatey A, Huang H, Zhou J, Lashley K, Chen Y, Christman M, Rotimi C: A genome-wide association study of hypertension and blood pressure in African Americans. PLoS Genet 5:e1000564, 2009
6. Zhao J, Bradfield JP, Zhang H, Annaiah K, Wang K, Kim CE, Glessner JT, Frackelton EC, Otieno FG, Doran J, Thomas KA, Garris M, Hou C, Chiavacci RM, Li M, Berkowitz RI, Hakonarson H, Grant S F A: Examination of all type 2 diabetes GWAS loci reveals HHEX-IDE as a locus influencing pediatric BMI. Diabetes 59:751-755, 2010
7. Böger CA, Gorski M, Li M, Hoffmann MM, Huang C, Yang Q, Teumer A, Krane V, O'Seaghdha CM, Kutalik Z, Wichmann H-E, Haak T, Boes E, Coassin S, Coresh J, Kollerits B, Haun M, Paulweber B, Köttgen A, Li G, Shlipak MG, Powe N, Hwang S-J, Dehghan A, Rivadeneira F, Uitterlinden A, Hofman A, Beckmann JS, Krämer BK, Witteman J, Bochud M, Siscovick D, Rettig R, Kronenberg F, Wanner C, Thadhani RI, Heid IM, Fox CS, Kao WH; CKDGen Consortium: Association of eGFRrelated loci identified by GWAS with incident CKD and ESRD. PLoS Genet 7:e1002292, 2011
8. Brown DM, Provoost AP, Daly MJ, Lander ES, Jacob HJ: Renal disease susceptibility and hypertension are under independent genetic control in the fawn-hooded rat. Nat Genet 12:44-51, 1996
9. Brown DM, Van Dokkum RP, Korte MR, McLauglin MG, Shiozawa M, Jacob HJ, Provoost AP: Genetic control of susceptibility for renal damage in hypertensive fawn-hooded rats. Ren Fail 20:407-411, 1998
10. Shiozawa M, Provoost AP, van Dokkum RP, Majewski RR, Jacob HJ: Evidence of gene-gene interactions in the genetic susceptibility to renal impairment after unilateral nephrectomy. J Am Soc Nephrol 11:2068-2078, 2000
11. Freedman BI, Rich SS, Yu H, Roh BH, Bowden DW: Linkage heterogeneity of end-stage renal disease on human chromosome 10. Kidney Int 62:770-774, 2002
12. Freedman BI: End-stage renal failure in African Americans: Insights in kidney disease susceptibility. Nephrol Dial Transplant 17:198-200, 2002
13. Hunt SC, Hasstedt SJ, Coon H, Camp NJ, Cawthon RM, Wu LL, Hopkins PN: Linkage of creatinine clearance to chromosome 10 in Utah pedigrees replicates a locus for end-stage renal disease in humans and renal failure in the fawn-hooded rat. Kidney Int 62:1143-1148, 2002
14. Schulz A, Litfin A, Kossmehl P, Kreutz R: Genetic dissection of increased urinary albumin excretion in the munich wistar frömter rat. J Am Soc Nephrol 13:2706-2714, 2002
15. Schulz A, Standke D, Kovacevic L, Mostler M, Kossmehl P, Stoll M, Kreutz R: A major gene locus links early onset albuminuria with renal interstitial fibrosis in the MWF rat with polygenetic albuminuria. J Am Soc Nephrol 14:3081-3089, 2003
16. St Lezin E, Griffin KA, Picken M, Churchill MC, Churchill PC, Kurtz TW, Liu W, Wang N, Kren V, Zidek V, Pravenec M, Bidani AK: Genetic isolation of a chromosome 1 region affecting susceptibility to hypertensioninduced renal damagein the spontaneously hypertensive rat. Hypertension 34:187-191, 1999
17. Yagil C, Sapojnikov M, Katni G, Ilan Z, Zangen SW, Rosenmann E, Yagil Y: Proteinuria and glomerulosclerosis in the Sabra genetic rat model of salt susceptibility. Physiol Genomics 9:167-178, 2002
18. Rangel-Filho A, Sharma M, Datta YH, Moreno C, Roman RJ, Iwamoto Y, Provoost AP, Lazar J, Jacob HJ: RF-2 gene modulates proteinuria and albuminuria independently of changes in glomerular permeability in the fawn-hooded hypertensive rat. J Am Soc Nephrol 16:852-856, 2005
19. Pereira-Leal JB, Seabra MC: Evolution of the Rab family of small GTPbinding proteins. J Mol Biol 313:889-901, 2001
20. Datta YH, Wu FC, Dumas PC, Rangel-Filho A, Datta MW, Ning G, Cooley BC, Majewski RR, Provoost AP, Jacob HJ: Genetic mapping and characterization of the bleeding disorder in the fawn-hooded hypertensive rat. Thromb Haemost 89:1031-1042, 2003
21. Loftus SK, Larson DM, Baxter LL, Antonellis A, Chen Y, Wu X, Jiang Y, Bittner M, Hammer JA 3rd, Pavan WJ: Mutation of melanosome protein RAB38 in chocolate mice. Proc Natl Acad Sci U S A 99:4471-4476, 2002
22. Oiso N, Riddle SR, Serikawa T, Kuramoto T, Spritz RA: The rat Ruby (R) locus is Rab38: Identical mutations in Fawn-hooded and Tester-Moriyama rats derived froman ancestral Long Evans rat sub-strain. MammGenome 15:307-314, 2004
23. Mátés L, Chuah M K L, Belay E, Jerchow B, Manoj N, Acosta-Sanchez A, Grzela DP, Schmitt A, Becker K, Matrai J, Ma L, Samara-Kuko E, Gysemans C, Pryputniewicz D, Miskey C, Fletcher B, Vanden Driessche T, Ivics Z, Izsvák Z: Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nat Genet 41:753-761, 2009
24. Geurts AM, Cost GJ, Freyvert Y, Zeitler B, Miller JC, Choi VM, Jenkins SS, Wood A, Cui X, Meng X, Vincent A, Lam S, Michalkiewicz M, Schilling R, Foeckler J, Kalloway S, Weiler H, Ménoret S, Anegon I, Davis GD, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Jacob HJ, Buelow R: Knockout rats via embryo microinjection of zinc-finger nucleases. Science 325:433, 2009
25. Hull RN, Cherry WR, Weaver GW: The origin and characteristics of a pig kidney cell strain, LLC-PK. In Vitro 12:670-677, 1976
26. Nielsen R, Birn H, Moestrup SK, Nielsen M, Verroust P, Christensen EI: Characterizationof a kidney proximal tubule cell line, LLC-PK1, expressing endocytotic active megalin. J Am Soc Nephrol 9:1767-1776, 1998
27. Ishibashi F: High glucose reduces albumin uptake in cultured proximal tubular cells (LLC-PK1). Diabetes Res Clin Pract 65:217-225, 2004
28. Caruso-Neves C, Kwon S-H, Guggino WB: Albumin endocytosis in proximal tubule cells is modulated by angiotensin II through an AT2 receptor-mediated protein kinase B activation. Proc Natl Acad Sci USA 102:17513-17518, 2005
29. Kriz W, Hosser H, Hähnel B, Gretz N, Provoost AP: From segmental glomerulosclerosis to total nephron degeneration and interstitial fibrosis: A histopathological study in rat models and human glomerulopathies. Nephrol Dial Transplant 13:2781-2798, 1998
30. Duclos S, Corsini R, Desjardins M: Remodeling of endosomes during lysosome biogenesis involves 'kiss and run' fusion events regulated by rab5. J Cell Sci 116:907-918, 2003
31. Weyer K, Storm T, Shan J, Vainio S, Kozyraki R, Verroust PJ, Christensen EI, Nielsen R: Mouse model of proximal tubule endocytic dysfunction. Nephrol Dial Transplant 26:3446-3451, 2011
32. Theilig F, Kriz W, Jerichow T, Schrade P, Hähnel B, Willnow T, Le Hir M, Bachmann S: Abrogation of protein uptake through megalin-deficient proximal tubules does not safeguard against tubulointerstitial injury. J Am Soc Nephrol 18:1824-1834, 2007
33. Carr G, Simmons N, Sayer J: A role for CBS domain 2 in trafficking of chloride channel CLC-5. BiochemBiophys Res Commun 310:600-605, 2003
34. Christensen EI, Devuyst O, Dom G, Nielsen R, Van der Smissen P, Verroust P, Leruth M, Guggino WB, Courtoy PJ: Loss of chloride channel ClC-5 impairs endocytosis by defective trafficking of megalin and cubilin in kidney proximal tubules. Proc Natl Acad Sci U S A 100:8472-8477, 2003
35. De Camilli P, Emr SD, McPherson PS, Novick P: Phosphoinositides as regulators in membrane traffic. Science 271:1533-1539, 1996
36. Devonald M A J, Karet FE: Renal epithelial traffic jams and one-way streets. J Am Soc Nephrol 15:1370-1381, 2004
37. Faucherre A, Desbois P, Satre V, Lunardi J, Dorseuil O, Gacon G: Lowe syndrome protein OCRL1 interacts with Rac GTPase in the trans-Golgi network. Hum Mol Genet 12:2449-2456, 2003
38. Kalatzis V, Cohen-Solal L, Cordier B, Frishberg Y, Kemper M, Nuutinen EM, Legrand E, Cochat P, Antignac C: Identification of 14 novel CTNS mutations and characterization of seven splice site mutations associated with cystinosis. Hum Mutat 20:439-446, 2002
39. Shotelersuk V, Larson D, Anikster Y, McDowell G, Lemons R, Bernardini I, Guo J, Thoene J, Gahl WA: CTNS mutations in an American-based population of cystinosis patients. Am J Hum Genet 63:1352-1362, 1998
40. Suchy SF, Olivos-Glander IM, Nussabaum RL: Lowe syndrome, a deficiency of phosphatidylinositol 4, 5-bisphosphate 5-phosphatase in the Golgi apparatus. Hum Mol Genet 4:2245-2250, 1995
41. Itagaki S, Shimamoto S, Hirano T, Iseki K, Sugawara M, Nishimura S, Fujimoto M, Kobayashi M, Miyazaki K: Comparison of urinary excretion of phenolsulfonphthalein in an animal model for Wilson's disease (Long-Evans Cinnamon rats) with that in normal Wistar rats: Involvement of primary active organic anion transporter. J Pharm Pharm Sci 7:227-234, 2004
42. Ninkovic I, White JG, Rangel-Filho A, Datta YH: The role of Rab38 in platelet dense granule defects. J Thromb Haemost 6:2143-2151, 2008
43. Zhang L, Yu K, Robert KW, De Bolt KM, Hong N, Tao J-Q, Fukuda M, Fisher AB, Huang S: Rab38 targets to lamellar bodies and normalizes their sizes in lung alveolar type II epithelial cells. Am J Physiol Lung Cell Mol Physiol 301:L461-L477, 2011
44. Niwa H, Yamamura K, Miyazaki J: Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193-199, 1991
45. Moreno C, Kaldunski ML, Wang T, Roman RJ, Greene AS, Lazar J, Jacob HJ, Cowley AW Jr: Multiple blood pressure loci on rat chromosome 13 attenuate development of hypertension in the Dahl S hypertensive rat. Physiol Genomics 31:228-235, 2007
46. Moffat J, Grueneberg DA, Yang X, Kim SY, Kloepfer AM, Hinkle G, Piqani B, Eisenhaure TM, Luo B, Grenier JK, Carpenter AE, Foo SY, Stewart SA, Stockwell BR, Hacohen N, Hahn WC, Lander ES, Sabatini DM, Root DE: A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124:1283-1298, 2006
47. Karolewski BA, Watson DJ, Parente MK, Wolfe JH: Comparison of transfection conditions for a lentivirus vector produced in large volumes. Hum Gene Ther 14:1287-1296, 2003
48. Morrison J, Knoll K, Hessner MJ, Liang M: Effect of high glucose on gene expression in mesangial cells: Upregulation of the thiol pathway is an adaptational response. Physiol Genomics 17:271-282, 2004
49. Winer J, Jung CK, Shackel I, Williams PM: Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction formonitoring gene expression in cardiac myocytes in vitro. Anal Biochem 270:41-49, 1999
50. Weichselbaum TE: An accurate and rapidmethod for the determination of proteins in small amounts of blood serum and plasma. Am J Clin Pathol 10:40-49, 1946
51. Kessler MA, Meinitzer A, Wolfbeis OS: Albumin blue 580 fluorescence assay for albumin. Anal Biochem 248:180-182, 1997
52. Moreno C, Williams JM, Lu L, Liang M, Lazar J, Jacob HJ, Cowley A W Jr, Roman RJ: Narrowing a region on rat chromosome 13 that protects against hypertension in Dahl SS-13BN congenic strains. Am J Physiol Heart Circ Physiol 300:H1530-H1535, 2011