Gene expression responses of threespine stickleback to salinity: Implications for salt-sensitive hypertension

Frontiers in Genetics

Volumn 5, Issue SEP, 2014, Pages

  Wang, Gang ^a   Yang, Ence ^a   Smith, Kerri J ^b   Zeng, Yong ^a,c   Ji, Guoli ^c   Connon, Richard ^d   Fangue, Nann A ^d   Cai, James J ^a,b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c XIAMEN UNIVERSITY   (China)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Differential expression; Gene environment interaction; mRNA sequencing; Salt handling; Salt responsive gene

Indexed keywords

EPITHELIAL SODIUM CHANNEL;

ADULT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATP1A1 GENE; BLOOD PRESSURE REGULATION; CLCN6 GENE; CLCNKA GENE; DIURESIS; EXTRACELLULAR SPACE; FEMALE; GASTEROSTEUS ACULEATUS; GENE; GENE EXPRESSION; GENE LOCUS; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; HOMEOSTASIS; HUMAN; HYPERTENSION; MAP3K15 GENE; MTHFR GENE; NONHUMAN; ORTHOLOGY; OVERLAPPING GENE; PHYLOGENY; PLOD1 GENE; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; SALT INTAKE; SALT STRESS; SGK1 GENE; SLC12A1 GENE; SLC12A3 GENE; WNK4 GENE;

ANIMALIA; GASTEROSTEUS;

EID: 84918839182     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2014.00312     Document Type: Article

References (64)

1. Albertson, R. C., Cresko, W., Detrich, H. W. 3rd., and Postlethwait, J. H. (2009). Evolutionary mutant models for human disease. Trends Genet. 25, 74-81. doi: 10.1016/j.tig.2008.11.006
2. Anders, S., and Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biol. 11:R106. doi: 10.1186/gb-2010-11-10-r106
3. Azizan, E. A., Poulsen, H., Tuluc, P., Zhou, J., Clausen, M. V., Lieb, A., et al. (2013). Somatic mutations in ATP1A1 and CACNA1D underlie a common subtype of adrenal hypertension. Nat. Genet. 45, 1055-1060. doi: 10.1038/ng.2716
4. Barrett, R. D., Paccard, A., Healy, T. M., Bergek, S., Schulte, P. M., Schluter, D., et al. (2011). Rapid evolution of cold tolerance in stickleback. Proc. Biol. Sci. 278, 233-238. doi: 10.1098/rspb.2010.0923
5. Becker, K. G., Barnes, K. C., Bright, T. J., and Wang, S. A. (2004). The genetic association database. Nat. Genet. 36, 431-432. doi: 10.1038/ng0504-431
6. Bystriansky, J. S., Richards, J. G., Schulte, P. M., and Ballantyne, J. S. (2006). Reciprocal expression of gill NaC/KC-ATPase alpha-subunit isoforms alpha 1a and alpha 1b during seawater acclimation of three salmonid fishes that vary in their salinity tolerance. J. Exp. Biol. 209, 1848-1858. doi: 10.1242/jeb.02188
7. Cheung, C. Y., and Ko, B. C. (2013). NFAT5 in cellular adaptation to hypertonic stress-regulations and functional significance. J. Mol. Signal. 8:5. doi: 10.1186/1750-2187-8-5
8. Colosimo, P. F., Hosemann, K. E., Balabhadra, S., Villarreal, G. Jr., Dickson, M., Grimwood, J., et al. (2005). Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307, 1928-1933. doi: 10.1126/science.1107239
9. Denton, D. A. (1982). The Hunger for Salt: An Anthropological, Physiological, and Medical Analysis. Berlin; New York: Springer-Verlag.
10. Dominiczak, A. F., and Munroe, P. B. (2010). Genome-wide association studies will unlock the genetic basis of hypertension: pro side of the argument. Hypertension 56, 1017-1020. discussion: 1025. doi: 10.1161/HYPERTENSIONAHA.110.156208
11. Evans, D. H. (2008). Teleost fish osmoregulation: what have we learned since August Krogh, Homer Smith, and Ancel Keys. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R704-R713. doi: 10.1152/ajpregu.90337.2008
12. Flicek, P., Amode, M. R., Barrell, D., Beal, K., Billis, K., Brent, S., et al. (2014). Ensembl 2014. Nucleic Acids Res. 42, D749-D755. doi: 10.1093/nar/gkt1196
13. Flister, M. J., Tsaih, S. W., O'Meara, C. C., Endres, B., Hoffman, M. J., Geurts, A. M., et al. (2013). Identifying multiple causative genes at a single GWAS locus. Genome Res. 23, 1996-2002. doi: 10.1101/gr.160283.113
14. Frisoli, T. M., Schmieder, R. E., Grodzicki, T., and Messerli, F. H. (2012). Salt and hypertension: is salt dietary reduction worth the effort? Am. J. Med. 125, 433-439. doi: 10.1016/j.amjmed.2011.10.023
15. Grøtan, K., Østbye, K., Taugbøl, A., and Vøllestad, L. A. (2012). No short-term effect of salinity on oxygen consumption in threespine stickleback (Gasterosteus aculeatus) from fresh, brackish, and salt water. Can. J. Zool. 90, 1386-1393. doi: 10.1139/cjz-2012-0121
16. Guyton, A. C., Coleman, T. G., Cowley, A. V. Jr., Scheel, K. W., Manning, R. D. Jr., and Norman, R. A. Jr. (1972). Arterial pressure regulation. Overriding dominance of the kidneys in long-term regulation and in hypertension. Am. J. Med. 52, 584-594. doi: 10.1016/0002-9343(72)90050-2
17. Haddy, F. J., and Pamnani, M. B. (1995). Role of dietary salt in hypertension. J. Am. Coll. Nutr. 14, 428-438. doi: 10.1080/07315724.1995.10718533
18. Halterman, J. A., Kwon, H. M., and Wamhoff, B. R. (2012). Tonicity-independent regulation of the osmosensitive transcription factor TonEBP (NFAT5). Am. J. Physiol. Cell Physiol. 302, C1-C8. doi: 10.1152/ajpcell.00327.2011
19. Hancock, A. M., Witonsky, D. B., Gordon, A. S., Eshel, G., Pritchard, J. K., Coop, G., et al. (2008). Adaptations to climate in candidate genes for common metabolic disorders. PLoS Genet. 4:e32. doi: 10.1371/journal.pgen.0040032
20. Hardcastle, T. J., and Kelly, K. A. (2010). baySeq: empirical Bayesian methods for identifying differential expression in sequence count data. BMC Bioinformatics 11:422. doi: 10.1186/1471-2105-11-422
21. Hastie, C. E., Padmanabhan, S., and Dominiczak, A. F. (2010). Genome-wide association studies of hypertension: light at the end of the tunnel. Int. J. Hypertens. 2010:509581. doi: 10.4061/2010/509581
22. Ho, J. E., Levy, D., Rose, L., Johnson, A. D., Ridker, P. M., and Chasman, D. I. (2011). Discovery and replication of novel blood pressure genetic loci in the Women's Genome Health Study. J. Hypertens. 29, 62-69. doi: 10.1097/HJH.0b013e3283406927
23. International Consortium for Blood Pressure Genome-Wide Association Studies. (2011). Genetic variants in novel pathways influence blood pressure and cardiovascular disease risk. Nature 478, 103-109. doi: 10.1038/nature10405
24. Jones, F. C., Grabherr, M. G., Chan, Y. F., Russell, P., Mauceli, E., Johnson, J., et al. (2012). The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55-61. doi: 10.1038/nature10944
25. Kato, N., Takeuchi, F., Tabara, Y., Kelly, T. N., Go, M. J., Sim, X., et al. (2011). Meta-analysis of genome-wide association studies identifies common variants associated with blood pressure variation in east Asians. Nat. Genet. 43, 531-538. doi: 10.1038/ng.834
26. Kingsley, D. M. (2003). Sequencing the Genome of Threespine Sticklebacks (Gasterosteus Aculeatus). Bethesda, MD: National Human Genome Research Institute (NHGRI) White Paper.
27. Kleinewietfeld, M., Manzel, A., Titze, J., Kvakan, H., Yosef, N., Linker, R. A., et al. (2013). Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature 496, 518-522. doi: 10.1038/nature11868
28. Kotchen, T. A., Cowley, A. W. Jr., and Frohlich, E. D. (2013). Salt in health and disease-a delicate balance. N. Engl. J. Med. 368, 1229-1237. doi: 10.1056/NEJMra1212606
29. Kozak, G. M., Brennan, R. S., Berdan, E. L., Fuller, R. C., and Whitehead, A. (2014). Functional and population genomic divergence within and between two species of killifish adapted to different osmotic niches. Evolution 68, 63-80. doi: 10.1111/evo.12265
30. Lamichhaney, S., Martinez Barrio, A., Rafati, N., Sundstrom, G., Rubin, C. J., Gilbert, E. R., et al. (2012). Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring. Proc. Natl. Acad. Sci. U.S.A. 109, 19345-19350. doi: 10.1073/pnas.1216128109
31. Le Bras, Y., Dechamp, N., Krieg, F., Filangi, O., Guyomard, R., Boussaha, M., et al. (2011). Detection of QTL with effects on osmoregulation capacities in the rainbow trout (Oncorhynchus mykiss). BMC Genet. 12:46. doi: 10.1186/1471-2156-12-46
32. Levy, D., Ehret, G. B., Rice, K., Verwoert, G. C., Launer, L. J., Dehghan, A., et al. (2009). Genome-wide association study of blood pressure and hypertension. Nat. Genet. 41, 677-687. doi: 10.1038/ng.384
33. Lieschke, G. J., and Currie, P. D. (2007). Animal models of human disease: zebrafish swim into view. Nat. Rev. Genet. 8, 353-367. doi: 10.1038/nrg2091
34. Lifton, R. P., Gharavi, A. G., and Geller, D. S. (2001). Molecular mechanisms of human hypertension. Cell 104, 545-556. doi: 10.1016/S0092-8674(01)00241-0
35. Luft, F. C., and Weinberger, M. H. (1982). Sodium intake and essential hypertension. Hypertension 4, III14-III19. doi: 10.1161/01.HYP.4.5_Pt_2.III14
36. McCairns, R. J., and Bernatchez, L. (2010). Adaptive divergence between freshwater and marine sticklebacks: insights into the role of phenotypic plasticity from an integrated analysis of candidate gene expression. Evolution 64, 1029-1047. doi: 10.1111/j.1558-5646.2009.00886.x
37. McCarron, D. A., Kazaks, A. G., Geerling, J. C., Stern, J. S., and Graudal, N. A. (2013). Normal range of human dietary sodium intake: a perspective based on 24-hour urinary sodium excretion worldwide. Am. J. Hypertens. 26, 1218-1223. doi: 10.1093/ajh/hpt139
38. McGurk, L., and Bonini, N. M. (2011). Cell biology. Yeast informs Alzheimer's disease. Science 334, 1212-1213. doi: 10.1126/science.1216073
39. Meneton, P., Jeunemaitre, X., De Wardener, H. E., and Macgregor, G. A. (2005). Links between dietary salt intake, renal salt handling, blood pressure, and cardiovascular diseases. Physiol. Rev. 85, 679-715. doi: 10.1152/physrev.00056.2003
40. Miller, C. T., Beleza, S., Pollen, A. A., Schluter, D., Kittles, R. A., Shriver, M. D., et al. (2007). cis-Regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131, 1179-1189. doi: 10.1016/j.cell.2007.10.055
41. Naguro, I., Umeda, T., Kobayashi, Y., Maruyama, J., Hattori, K., Shimizu, Y., et al. (2012). ASK3 responds to osmotic stress and regulates blood pressure by suppressing WNK1-SPAK/OSR1 signaling in the kidney. Nat. Commun. 3:1285. doi: 10.1038/ncomms2283
42. Newton-Cheh, C., Johnson, T., Gateva, V., Tobin, M. D., Bochud, M., Coin, L., et al. (2009). Genome-wide association study identifies eight loci associated with blood pressure. Nat. Genet. 41, 666-676. doi: 10.1038/ng.361
43. Niu, C. J., Rummer, J. L., Brauner, C. J., and Schulte, P. M. (2008). Heat shock protein (Hsp70) induced by a mild heat shock slightly moderates plasma osmolarity increases upon salinity transfer in rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 148, 437-444. doi: 10.1016/j.cbpc.2008.04.011
44. Norman, J. D., Danzmann, R. G., Glebe, B., and Ferguson, M. M. (2011). The genetic basis of salinity tolerance traits in Arctic charr (Salvelinus alpinus). BMC Genet. 12:81. doi: 10.1186/1471-2156-12-81
45. Ohta, A., Rai, T., Yui, N., Chiga, M., Yang, S. S., Lin, S. H., et al. (2009). Targeted disruption of the Wnk4 gene decreases phosphorylation of Na-Cl cotransporter, increases Na excretion and lowers blood pressure. Hum. Mol. Genet. 18, 3978-3986. doi: 10.1093/hmg/ddp344
46. Oi, K., Sohara, E., Rai, T., Misawa, M., Chiga, M., Alessi, D. R., et al. (2012). A minor role of WNK3 in regulating phosphorylation of renal NKCC2 and NCC co-transporters in vivo. Biol. Open 1, 120-127. doi: 10.1242/bio.2011048
47. O'Shaughnessy, K. M., and Karet, F. E. (2006). Salt handling and hypertension. Annu. Rev. Nutr. 26, 343-365. doi: 10.1146/annurev.nutr.26.061505.111316
48. O'Shea, J. J., and Jones, R. G. (2013). Autoimmunity: rubbing salt in the wound. Nature 496, 437-439. doi: 10.1038/nature11959
49. Padmanabhan, S., Newton-Cheh, C., and Dominiczak, A. F. (2012). Genetic basis of blood pressure and hypertension. Trends Genet. 28, 397-408. doi: 10.1016/j.tig.2012.04.001
50. Pei, D. S., Sun, Y. H., Chen, S. P., Wang, Y. P., Hu, W., and Zhu, Z. Y. (2007). Zebrafish GAPDH can be used as a reference gene for expression analysis in cross-subfamily cloned embryos. Anal. Biochem. 363, 291-293. doi: 10.1016/j.ab.2006.12.005
51. Pravenec, M., and Kurtz, T. W. (2010). Recent advances in genetics of the spontaneously hypertensive rat. Curr. Hypertens. Rep. 12, 5-9. doi: 10.1007/s11906-009-0083-9
52. Rapp, J. P. (1982). Dahl salt-susceptible and salt-resistant rats. A review. Hypertension 4, 753-763. doi: 10.1161/01.HYP.4.6.753
53. Rengmark, A. H., Slettan, A., Lee, W. J., Lie, Ø., and Lingaas, F. (2007). Identification and mapping of genes associated with salt tolerance in tilapia. J. Fish Biol. 71, 409-422. doi: 10.1111/j.1095-8649.2007.01664.x
54. Robinson, M. D., McCarthy, D. J., and Smyth, G. K. (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140. doi: 10.1093/bioinformatics/btp616
55. Ruiter, A. J. H. D., and Bonga, S. E. W. (1985). Consequences of nestbuilding behaviour for osmoregulation in male three-spined sticklebacks. Behaviour 93, 8-20. doi: 10.1163/156853986X00694
56. Scott, G. R., Richards, J. G., Forbush, B., Isenring, P., and Schulte, P. M. (2004). Changes in gene expression in gills of the euryhaline killifish Fundulus heteroclitus after abrupt salinity transfer. Am. J. Physiol. Cell Physiol. 287, C300-C309. doi: 10.1152/ajpcell.00054.2004
57. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D. R., et al. (2012). Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578. doi: 10.1038/nprot.2012.016
58. Vilella, A. J., Severin, J., Ureta-Vidal, A., Heng, L., Durbin, R., and Birney, E. (2009). EnsemblCompara Genetrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res. 19, 327-335. doi: 10.1101/gr.073585.107
59. Wain, L. V., Verwoert, G. C., O'Reilly, P. F., Shi, G., Johnson, T., Johnson, A. D., et al. (2011). Genome-wide association study identifies six new loci influencing pulse pressure and mean arterial pressure. Nat. Genet. 43, 1005-1011. doi: 10.1038/ng.922
60. Whitehead, A., Roach, J. L., Zhang, S., and Galvez, F. (2011). Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient. Proc. Natl. Acad. Sci. U.S.A. 108, 6193-6198. doi: 10.1073/pnas.1017542108
61. Whitehead, A., Roach, J. L., Zhang, S. J., and Galvez, F. (2012). Salinity- and population-dependent genome regulatory response during osmotic acclimation in the killifish (Fundulus heteroclitus) gill. J. Exp. Biol. 215, 1293-1305. doi: 10.1242/jeb.062075
62. Wu, C., Yosef, N., Thalhamer, T., Zhu, C., Xiao, S., Kishi, Y., et al. (2013). Induction of pathogenic TH17 cells by inducible salt-sensing kinase SGK1. Nature 496, 513-517. doi: 10.1038/nature11984
63. Wulff, P., Vallon, V., Huang, D. Y., Volkl, H., Yu, F., Richter, K., et al. (2002). Impaired renal Na(C) retention in the sgk1-knockout mouse. J. Clin. Invest. 110, 1263-1268. doi: 10.1172/JCI0215696
64. Xu, G., Deng, N., Zhao, Z., Judeh, T., Flemington, E., and Zhu, D. (2011). SAMMate: a GUI tool for processing short read alignments in SAM/BAM format. Source Code Biol. Med. 6:2. doi: 10.1186/1751-0473-6-2