Theoretical model for gene-gene, gene-environment, and gene-sex interactions based on congenic-strain analysis of blood pressure in Dahl salt-sensitive rats

Physiological Genomics

Volumn 45, Issue 16, 2013, Pages 737-750

  Rapp, John P ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

Epistasis; Genetic hypertension; QTL; Quantitative trait loci; Saltsensitive hypertension

Indexed keywords

ALLELE; ANIMAL EXPERIMENT; ARTICLE; BLOOD PRESSURE REGULATION; CHROMOSOME SEGREGATION; CONGENIC STRAIN; DAHL SALT SENSITIVE RAT; EPISTASIS; GENE INTERACTION; GENE MAPPING; GENETIC ANALYSIS; GENOTYPE ENVIRONMENT INTERACTION; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; RAT; SEX LINKAGE; THEORETICAL MODEL;

EID: 84882630408     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00046.2013     Document Type: Article

References (79)

1. Anderson JC, Voigt CA, Arkin A. Environmental signal integration by a modular AND gate. Mol Syst Biol 3: 1-8, 2007.
2. Ariyarajah A, Palijan A, Dutil J, Prithivira K, Deng Y, Deng AY. Dissecting quantitative trait loci into opposite blood pressure effects on Dahl rat chromosome 8 by congenic strains. J Hypertens 22: 1495-1502, 2004.
3. Biesiadecki ABJ, Schneider KL, Yu ZB, Chong SM, Jin JP. An R111C polymorphism in wild turkey cardiac troponin I accompanying the dilated cardiomyopathy-related abnormal splicing variant of cardiac troponin T with potentially compensatory effects. J Biol Chem 279: 13825-13832, 2004.
4. Carlborg O, Haley CS. Epistasis: too often neglected in complex trait studies? Nat Rev Genet 5: 618-625, 2004.
5. Charpentier S, Jarvie KR, Severynse DM, Caron MG, Tiberi M. Silencing of the constitutive activity of the dopamine D1B receptor. J Biol Chem 271: 28071-28076, 1996.
6. Charron S, Duong C, Menard A, Roy J, Eliopoulos V, Lambert R, Deng AY. Epistasis, not numbers, regulates functions of clustered Dahl rat quantitative trait loci applicable to human hypertension. Hypertension 46: 1300-1308, 2005.
7. Charron S, Lambert R, Eliopoulos V, Duong C, Menard A, Roy J, Deng AY. A loss of genome buffering capacity of Dahl salt-sensitive model to modulate blood pressure as a cause of hypertension. Hum Mol Genet 14: 3877-3884, 2005.
8. Chauvet C, Charron S, Menard A, Xiao C, Roy J, Deng AY. Submegabase resolution of epistatically interacting quantitative trait loci for blood pressure applicable for essential hypertension. J Hypertens 26: 893-901, 2008.
9. Chauvet C, Crespo K, Menard A, Wu Y, Xiao C, Blain M, Roy J, Deng AY. α-Kinase 2 is a novel candidate gene for inherited hypertension in Dahl rats. Hypertension 29: 1320-1326, 2011.
10. Chauvet C, Menard A, Tremblay J, Xiao C, Shi Y, L'Heureux Cardin S, Tardif JC, Nattel S, Deng AY. Cardiac pathways distinguish two epistatic modules enacting BP quantitative trait loci and candidate gene analysis. Hypertens Res 32: 631-637, 2009.
11. Cicila GT, Garrett MR, Lee SJ, Liu J, Dene H, Rapp JP. High resolution mapping of the blood pressure QTL on chromosome 7 using Dahl rat congenic strains. Genomics 72: 51-60, 2001.
12. Cicila GT, Morgan EE, Lee SJ, Frams P, Yerga-Woolwine S, Toland EJ, Ramdath RS, Gopalakrishnan K, Buhman K, Nestor-Kalinoski AL, Khuder SA, Joe B. Epistatic genetic determinants of blood pressure and mortality in a salt-sensitive hypertension model. Hypertension 53: 725-732, 2009.
13. Cicila GT, Rapp JP, Bloch KD, Kurtz TW, Pravenec M, Kren V, Hong CC, Quertermous T, Ng SC. Cosegregation of the encothelin-3 locus with blood pressure and relative heart weight in inbred Dahl rats. J Hypertens 12: 634-631, 1994.
14. Cicila GT, Rapp JP, Wang JM, St. Lezin E, Ng SC, Kurtz TW. Linkage of 11β-hydroxylase mutations with altered steroid biosynthesis and blood pressure in the Dahl rat. Nat Genet 3: 346-353, 1993.
15. Cowley AW, Roman RJ, Kaldunski ML, Dumas P, Dickhout JG, Greene AS, Jacob HJ. Brown Norway chromosome 13 confers protection from high salt to consomic Dahl rat. Hypertension 37: 456-461, 2001.
16. Cowley AW, Stoll M, Green AS, Kaldunski ML, Roman RJ, Tonellato PJ, Schork NJ, Dumas P, Jacob HJ. Genetically defined risk of salt sensitivity in an intercross of Brown Norway and Dahl S rats. Physiol Genomics 2: 107-115, 2000.
17. Crespo K, Chauvet C, Blain M, Menard A, Roy J, Deng AY. Normotension in Lewis and Dahl salt-sensitive rats is governed by different genes. Hypertension 29: 460-465, 2011.
18. Dahl LK, Heine M, Tassinari L. Role of genetic factors to genetic susceptibility to experimental hypertension due to chronic excess salt ingestion. Nature 194: 480-482, 1962.
19. Dahl LK, Heine M, Tassinari L. Effects of chronic excess salt ingestion. J Exp Med 115: 1173-1190, 1962.
20. Deng AY, Dene H, Rapp JP. Congenic strains for the blood pressure quantitative trait locus on rat chromosome 2. Hypertension 30: 199-202, 1997.
21. Deng AY, Menard A, Xiao C, Roy J. Sexual dimorphism on hypertension of quantitative trait loci entrapped in Dahl congenic rats. Clin Exp Hypertens 30: 511-519, 2008.
22. Dukhanina OI, Dene H, Deng AY, Choi CR, Hoebee B, Rapp JP. Linkage map and congenic strains to localize blood pressure QTL on rat chromosome 10. Mamm Genome 8: 229-235, 1997.
23. Dutil J, Deng AY. Further chromosomal mapping of a blood pressure QTL in Dahl rats on chromosome 2 using congenic strains. Physiol Genomics 6: 3-9, 2001.
24. Dutil J, Eliopoulos V, Tremblay J, Hamet P, Charron S, Deng AY. Multiple quantitative trait loci for blood pressure interacting epistatically and additively on Dahl rat chromosome 2. Hypertension 45: 557-564, 2005.
25. Eliopoulos V, Dutil J, Deng Y, Grondin M, Deng AY. Severe hypertension caused by alleles from normotensive Lewis for a quantitative trait locus on chromosome 2. Physiol Genomics 22: 70-75, 2005.
26. Flister MJ, Prisco SZ, Sarkis AB, O'Meara CC, Hoffman M, Wendt-Andrae J, Moreno C, Lazar J, Jacob HJ. Identification of hypertension susceptibility loci on rat chromosome 12. Hypertension 60: 942-948, 2012.
27. Garrett MR, Dene H, Walder R, Zhang QY, Cicila GT, Assidnia S, Deng AY, Rapp JP. Genome scan and congenic strains for blood pressure QTL using Dahl salt-sensitive rats. Genome Res 8: 711-723, 1998.
28. Garrett MR, Joe B, Dene H, Rapp JP. Identification of blood pressure quantitative trait loci that differentiate two hypertensive strains. J Hypertens 20: 2399-2406, 2002.
29. Garrett MR, Meng H, Rapp JP, Joe B. Locating a blood pressure quantitative trait locus within 117 kb on the rat genome. Hypertension 45: 451-459, 2005.
30. Garrett MR, Rapp JP. Two closely linked interactive blood pressure QTL on rat chromosome 5 defined using congenic Dahl rats. Physiol Genomics 8: 81-86, 2002.
31. Garrett MR, Rapp JP. Multiple blood pressure QTL on rat chromosome 2 defined by congenic Dahl rats. Mamm Genome 13: 41-44, 2002.
32. Garrett MR, Rapp JP. Defining the blood pressure QTL on chromosome 7 in Dahl rats by a 177-kb congenic segment containing Cyp11b1. Mamm Genome 14: 268-273, 2003.
33. Garrett MR, Saad Y, Dene H, Rapp JP. Blood pressure QTL that differentiate Dahl salt-sensitive and spontaneously hypertensive rats. Physiol Genomics 3: 33-38, 2000.
34. Garrett MR, Zhang X, Dukhanina OI, Deng AY, Rapp JP. Two linked blood pressure quantitative trait loci on chromosome 10 defined by Dahl rat congenic strains. Hypertension 38: 779-786, 2001.
35. Gibson G, Dworkin I. Uncovering cryptic genetic variation. Nat Rev Genet 5: 681-690, 2004.
36. Gopalakrishnan K, Kumarasamy S, Abdul-Majeed S, Kalinoski A, Morgan EE, Gohara AF, Nauli SM, Filipiak WE, Saunders TL, Joe B. Targeted disruption of Adamts16 gene in a rat genetic model of hypertension. Proc Natl Acad Sci USA 109: 20555-20559, 2012.
37. Gopalakrishnan K, Kumarasamy S, Yan Y, Liu J, Kalinoski A, Kothandapani A, Farms P, Joe B. Increased expression of rififylin in a <330 kb congenic strain is linked to impaired endosomal recycling in proximal tubules. Front Genet 3: 1-14, 2012.
38. Gopalakrishnan K, Morgan EE, Yerga-Woolwie S, Farms P, Kumarasamy S, Kalinoski A, Liu X, Wu J, Liu L, Joe B. Augmented rififylin is a risk factor linked to aberrant cardiomyocyte function, short-QT interval and hypertension. Hypertension 57: 764-771, 2011.
39. Gopalakrishnan K, Saikumar J, Peters CG, Kumarasamy S, Farms P, Yerga-Woolwie S, Toland EJ, Schnackel W, Giovannucci DR, Joe B. Defining a rat blood pressure quantitative locus to a <81.8 kb congenic segment: comprehensive sequencing and renal transcriptome analysis. Physiol Genomics 42A: 153-161, 2010.
40. Groudin M, Eliopoulos V, Lambert R, Deng Y, Ariyarajah A, Moujahidine M, Dutil J, Charron S, Deng AY. Complete and overlapping congenics proving the existence of a quantitative trait locus for blood pressure on Dahl rat chromosome 17. Physiol Genomics 21: 112-116, 2005.
41. Guyton AC. Long-term arterial pressure control: an analysis from animal experiments and computer and graphic models. Am J Physiol Regul Integr Comp Physiol 259: R865-R877, 1990.
42. Guyton AC. Blood pressure control-special role of the kidneys and body fluids. Science 252: 1813-1816, 1991.
43. Guyton AC, Coleman TG, Cowley AW, Manning RD, Norman RA, Ferguson JD. A systems analysis approach to understanding long-range arterial blood pressure control and hypertension. Circ Res 35: 159-176, 1974.
44. Herrera VL, Pasion KA, Moran AM, Ruiz-Opazo N. Dahl (S × R) congenic strain analysis confirms and defines a chromosome 5 femalespecific blood pressure quantitative trait locus to <7 Mbp. PLoS One 7: e42214, 2013.
45. Herrera VL, Tsikoudakis A, Pouce LRB, Matsubara Y, Ruiz-Opazo N. Sex-specific QTLs and interacting loci underlie salt-sensitive hypertension and target organ complications in Dahl S/JrHS hypertensive rats. Physiol Genomics 26: 172-179 2006.
46. + in 2 congenic strains of Dahl salt-sensitive rats. Hypertension 49: 1315-1320, 2007.
47. +] precede the increases in blood pressure in Dahl S rats and SHR on a high-salt diet. Am J Physiol Heart Circ Physiol 287: H1160-H1166, 2004.
48. Joe B, Garrett MR, Dene H, Rapp JP. Substitution mapping of a blood pressure quantitative trait locus to a 2.73 Mb region on rat chromosome 1. J Hypertens 21: 2077-2084, 2003.
49. Joe B, Saad Y, Lee NH, Frank BC, Achinike OH, Luu TV, Gopalakrishnan K, Toland EJ, Farms P, Yerga-Woolwine S, Manickavasagam E, Rapp JP, Garrett MR, Coe D, Apte SS, Rankinen T, Perusse L, Ehret GB, Ganssh SK, Cooper RS, O'Connor A, Rice T, Weder AB, Chakravarti A, Rao DC, Bouchard C. Positional identification of variants of Adamts16 linked to inherited hypertension. Hum Mol Genet 18: 2825-2838, 2009.
50. Kato N, Hyne G, Bihoreau MT, Gauguier D, Lathrop GM, Rapp JP. Complete genome searches for quantitative trait loci controlling blood pressure and related traits in four segregating populations derived from Dahl hypertensive rats. Mamm Genome 10: 259-265, 1999.
51. Kroymann J, Mitchell-Olds T. Epistasis and balanced polymorphism influencing complex trait variation. Nature 435: 95-98, 2005.
52. Kumarasamy S, Gopalakrishnan K, Toland ET, Yerga-Woolsine S, Farms P, Morgan EE, Joe B. Refined mapping of blood pressure quantitative trait loci using congenic strains developed from two genetically hypertensive rat models. Hypertens Res 34: 1263-1270, 2011.
53. Lehner B. Molecular mechanisms of epistasis within and between genes. Trends Genet 27: 323-331, 2011.
54. Liti G, Louis EJ. Advances in quantitative trait analysis in yeast. PLoS Genet 8: e1002912, 2012.
55. Mattson DL, Dwinell MR, Greene AS, Kwitek AE, Roman RJ, Jacob HJ, Cowley AW. Chromosome substitution reveals the genetic basis of Dahl salt-sensitive hypertension and renal disease. Am J Physiol Renal Physiol 295: F837-F842, 2008.
56. Mattson DL, Kunert MP, Kaldunski ML, Greene AS, Roman RJ, Jacob HJ, Cowley AW. Influence of diet and genetics on hypertension and renal disease in Dahl salt-sensitive rats. Physiol Genomics 16: 194-203, 2004.
57. Mattson DL, Meister CJ, Marcelle ML. Dietary protein source determines the degree of hypertension and renal disease in the Dahl saltsensitive rat. Hypertension 45: 736-741, 2005.
58. Meng H, Garrett MR, Dene H, Rapp JP. Localization of a blood pressure QTL to a 2.4-cM interval on rat chromosome 9 using congenic strains. Genomics 81: 210-220, 2003.
59. Moreno C, Kaldunski ML, Wang T, Roman RJ, Greene AS, Lazar J, Jacob HJ, Cowley AW. Multiple blood pressure loci on rat chromosome 13 attenuate development of hypertension in the Dahl S hypertensive rat. Physiol Genomics 31: 228-235, 2007.
60. Moujahidine M, Dutil J, Hamet P, Deng AY. Congenic mapping of a blood pressure QTL on chromosome 16 of Dahl rats. Mamm Genome 13: 153-156, 2002.
61. Palijan A, Dutil J, Deng AY. Quantitative trait loci with opposing blood pressure effects demonstrating epistasis on Dahl rat chromosome 3. Physiol Genomics 15: 1-8, 2003.
62. Phillips PC. Epistasis-the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet 9: 855-867, 2008.
63. Rapp JP, Dene H. Development and characterization of inbred strains of Dahl salt-sensitive and salt-resistant rats. Hypertension 7: 340-349, 1985.
64. Rapp JP, Garrett MR, Deng AY. Construction of a double congenic strain to prove an epistatic interaction on blood pressure between rat chromosomes 2 and 10. J Clin Invest 101: 1591-1595, 1998.
65. Rapp JP, Joe B. Use of contiguous congenic strains in analyzing compound QTLs. Physiol Genomics 44: 117-120, 2012.
66. Rapp JP, Wang SW, Dene H. Effect of genetic background on cosegregation of rennin alleles and blood pressure in Dahl rats. Am J Hypertens 3: 391-396, 1990.
67. Saad Y, Garrett MR, Lee SJ, Dene H, Rapp JP. Localization of a blood pressure QTL on rat chromosome 1 using Dahl congenic rats. Physiol Genomics 1: 119-125, 1999.
68. Saad Y, Garrett MR, Manickavagam E, Yerga-Woolwine S, Farms P, Radecki T, Joe B. Fine mapping and comprehensive transcript analysis reveals nonsynonymous variants within a novel 1.17 Mb blood pressure QTL region on rat chromosome 10. Genomics 89: 343-353, 2007.
69. Saad Y, Garrett MR, Rapp JP:. Multiple blood pressure QTL on rat chromosome 1 defined by Dahl rat congenic strains. Physiol Genomics 4: 201-214, 2001.
70. Saad Y, Yerga-Woolwine S, Saikumar J, Farms P, Manickavasagam E, Toland EJ, Joe B. Congenic interval mapping of RNO10 reveals a complex cluster of closely-linked genetic determinants of blood pressure. Hypertension 50: 891-898, 2007.
71. Schlager G, Chao CS. The role of dominance and epistasis in the genetic control of blood pressure in rodent models of hypertension. Clin Exp Hypertens Theor Pract A13: 947-953, 1991.
72. Shao H, Burrage LC, Sinasac DS, Hill AE, Ernest SR, O'Brien W, Courtland HW, Jepsen KJ, Kirby A, Kulbokas EJ, Daly MJ, Broman KW, Lander ES, Nadeau JH. Genetic architecture of complex traits: large phenotypic effects and pervasive epistasis. Proc Natl Acad Sci USA 105: 19910-19914, 2008.
73. 4 in carbamylcholine induced gallbladder contractility. J Pharmacol Exp Therapeut 301: 643-650, 2002.
74. Tamsir A, Tabor JJ, Voigt CA. Robust multicellular computing using genetically encoded NOR gates and chemical "wires". Nature 469: 212-215, 2011.
75. Toland EJ, Saad Y, Yerga-Woolwine S, Ummel S, Farms P, Ramdath R, Frank BC, Lee NH, Joe B. Closely linked non-additive blood pressure quantitative trait loci. Mamm Genome 19: 209-218, 2008.
76. Toland EJ, Yerga-Woolwine S, Farms P, Cicila GT, Saad Y, Joe B. Blood pressure and proteinuria effects of multiple quantitative trait loci on rat chromosome 9 that differentiate the spontaneously hypertensive rat from the Dahl salt-sensitive rat. J Hypertens 26: 2134-2141, 2008.
77. Wendt N, Shulz A, Siegel A, Weiss J, Wehland M, Sietmann A, Kossmehl P, Grimm D, Stoll M, Kreutz R. Rat chromosome 19 transfer from SHR ameliorates hypertension, salt-sensitivity, cardiovascular and renal organ damage in salt-sensitive Dahl rats. J Hypertens 25: 95-102, 2007.
78. Zhou M, Reznikoff WS. Tn5 transposase mutants that alter DNA binding specificity. J Mol Biol 271: 362-373, 1997.
79. Zuk O, Hechter E, Sunyaev SR, Lander ES. The mystery of missing heritability: Genetic interactions create phantom heritability. Proc Natl Acad Sci USA 109: 1193-1198, 2012.