Identification and prioritization of NUAK1 and PPP1CC as positional candidate loci for skeletal muscle strength phenotypes

Physiological Genomics

Volumn 43, Issue 17, 2011, Pages 981-992

  Windelinckx, An ^a   de Mars, Gunther ^a   Huygens, Wim ^a   Peeters, Maarten W ^a   Vincent, Barbara ^a   Wijmenga, Cisca ^b   Lambrechts, Diether ^a   Aerssens, Jeroen ^c   Vlietinck, Robert ^a   Beunen, Gaston ^a   Thomis, Martine A I ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c Tibotec VIRCO Virology bvba   (Belgium)

Author keywords

Complex trait; Family based association; Genotype phenotype association

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CALCIUM ION; PHOSPHOPROTEIN PHOSPHATASE 1;

ARTICLE; CALCIUM TRANSPORT; CHROMOSOME 12Q; CONTROLLED STUDY; FOLLOW UP; GENE LOCUS; GENE MAPPING; GENETIC ASSOCIATION; HEART MUSCLE; HUMAN; HUMAN TISSUE; MALE; MUSCLE STRENGTH; NUAK1 GENE; PHENOTYPE; PPP1CC GENE; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; SINGLE NUCLEOTIDE POLYMORPHISM; SKELETAL MUSCLE; TORQUE;

ADOLESCENT; ADULT; GENOTYPE; HUMANS; MALE; MUSCLE STRENGTH; MUSCLE, SKELETAL; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN KINASES; PROTEIN PHOSPHATASE 1; REPRESSOR PROTEINS; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; YOUNG ADULT;

EID: 80052576924     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00200.2010     Document Type: Article

References (64)

1. Abecasis GR, Cherny SS, Cookson WO, Cardon LR. Merlin-rapid analysis of dense genetic maps using sparse gene flow trees. Nat Genet 30: 97-101, 2002.
2. Abecasis GR, Noguchi E, Heinzmann A, Traherne JA, Bhattacharyya S, Leaves NI, Anderson GG, Zhang Y, Lench NJ, Carey A, Cardon LR, Moffatt MF, Cookson WO. Extent and distribution of linkage disequilibrium in three genomic regions. Am J Hum Genet 68: 191-197, 2001.
3. Aerts S, Lambrechts D, Maity S, Van Loo P, Coessens B, De Smet F, Tranchevent LC, De Moor B, Marynen P, Hassan B, Carmeliet P, Moreau Y. Gene prioritization through genomic data fusion. Nat Biotechnol 24: 537-544, 2006.
4. Ardlie K, Liu-Cordero SN, Eberle MA, Daly M, Barrett J, Winchester E, Lander ES, Kruglyak L. Lower-than-expected linkage disequilibrium between tightly linked markers in humans suggests a role for gene conversion. Am J Hum Genet 69: 582-589, 2001.
5. Ardlie KG, Kruglyak L, Seielstad M. Patterns of linkage disequilibrium in the human genome. Nat Rev Genet 3: 299-309, 2002.
6. Arsic N, Zacchigna S, Zentilin L, Ramirez-Correa G, Pattarini L, Salvi A, Sinagra G, Giacca M. Vascular endothelial growth factor stimulates skeletal muscle regeneration in Vivo. Mol Ther 10: 844-854, 2004.
7. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263-265, 2005.
8. Barton ER. The ABCs of IGF-I isoforms: impact on muscle hypertrophy and implications for repair. Appl Physiol Nutr Metab 31: 791-797, 2006.
9. Beohar N, Kawamoto S. Transcriptional regulation of the human nonmuscle myosin II heavy chain-A gene. Identification of three clustered cis-elements in intron-1 which modulate transcription in a cell type- and differentiation state-dependent manner. J Biol Chem 273: 9168-9178, 1998.
10. 2 uptake response to standardized exercise training programs. J Appl Physiol 110: 1160-1170, 2011.
11. Bray MS, Hagberg JM, Perusse L, Rankinen T, Roth SM, Wolfarth B, Bouchard C. The human gene map for performance and health-related fitness phenotypes: the 2006-2007 update. Med Sci Sports Exerc 41: 35-73, 2009.
12. Collins A, Lonjou C, Morton NE. Genetic epidemiology of singlenucleotide polymorphisms. Proc Natl Acad Sci USA 96: 15173-15177, 1999.
13. de Bakker PI, Yelensky R, Pe'er I, Gabriel SB, Daly MJ, Altshuler D. Efficiency and power in genetic association studies. Nat Genet 37: 1217-1223, 2005.
14. De Mars G, Windelinckx A, Huygens W, Peeters MW, Beunen GP, Aerssens J, Vlietinck R, Thomis MAI. Genome-wide linkage scan for maximum and length-dependent knee muscle strength in young men: significant evidence for linkage at chromosome 14q24.3. J Med Genet 45: 275-283, 2008.
15. De Mars G, Windelinckx A, Huygens W, Peeters MW, Beunen GP, Aerssens J, Vlietinck R, Thomis MA. Genome-wide linkage scan for contraction velocity characteristics of knee musculature in the Leuven Genes for Muscular Strength Study. Physiol Genomics 35: 36-44, 2008.
16. Duvigneaud N, Matton L, Wijndaele K, Deriemaeker P, Lefevre J, Philippaerts R, Thomis M, Delecluse C, Duquet W. Relationship of obesity with physical activity, aerobic fitness and muscle strength in Flemish adults. J Sports Med Phys Fitness 48: 201-210, 2008.
17. Evans DM, Cardon LR. Guidelines for genotyping in genomewide linkage studies: single-nucleotide-polymorphism maps versus microsatellite maps. Am J Hum Genet 75: 687-692, 2004.
18. Fisher JS, Ju JS, Oppelt PJ, Smith JL, Suzuki A, Esumi H. Muscle contractions, AICAR, and insulin cause phosphorylation of an AMPKrelated kinase. Am J Physiol Endocrinol Metab 289: E986-E992, 2005.
19. Hagberg JM, Rankinen T, Loos R, Perusse L, Roth SM, Wolfarth B, Bouchard C. Advances in exercise, fitness, and performance genomics in 2010. Med Sci Sports Exerc 43: 743-752, 2011.
20. Hoppe PE, Chau J, Flanagan KA, Reedy AR, Schriefer LA. C. elegans unc-82 encodes a serine/threonine kinase important for myosin filament organization in muscle during growth. Genetics 184: 79-90, 2010.
21. Horvath S, Xu X, Laird NM. The family based association test method: strategies for studying general genotype-phenotype associations. Eur J Hum Genet 9: 301-306, 2001.
22. Horvath S, Xu X, Lake SL, Silverman EK, Weiss ST, Laird NM. Family-based tests for associating haplotypes with general phenotype data: application to asthma genetics. Genet Epidemiol 26: 61-69, 2004.
23. Huygens W, Thomis MA, Peeters MW, Aerssens J, Janssen R, Vlietinck R, Beunen G. Linkage of myostatin pathway genes with knee strength in humans. Physiol Genomics 17: 264-270, 2004.
24. Huygens W, Thomis MA, Peeters MW, Aerssens J, Janssen R, Vlietinck RF, Beunen G. A quantitative trait locus on 13q14.2 for trunk strength. Twin Res 7: 603-606, 2004.
25. Huygens W, Thomis MA, Peeters MW, Vlietinck RF, Beunen GP. Determinants and upper-limit heritabilities of skeletal muscle mass and strength. Can J Appl Physiol 29: 186-200, 2004.
26. Huygens W, Thomis MAI, Peeters MW, Aerssens J, Vlietinck R, Beunen GP. Quantitative trait loci for human muscle strength: linkage analysis of myostatin pathway genes. Physiol Genomics 22: 390-397, 2005.
27. Karasik D, Kiel DP. Genetics of the musculoskeletal system: a pleiotropic approach. J Bone Miner Res 23: 788-802, 2008.
28. Kong X, Murphy K, Raj T, He C, White PS, Matise TC. A combined linkage-physical map of the human genome. Am J Hum Genet 75: 1143-1148, 2004.
29. Kunst G, Kress KR, Gruen M, Uttenweiler D, Gautel M, Fink RHA. Myosin binding protein C, a phosphorylation-dependent force regulator in muscle that controls the attachment of myosin heads by its interaction with myosin S2. Circ Res 86: 51-58, 2000.
30. Laird NM, Horvath S, Xu X. Implementing a unified approach to family-based tests of association. Genet Epidemiol 19, Suppl 1: S36-S42, 2000.
31. Landers KA, Hunter GR, Wetzstein CJ, Bamman MM, Weinsier RL. The interrelationship among muscle mass, strength, and the ability to perform physical tasks of daily living in younger and older women. J Gerontol A Biol Sci Med Sci 56: B443-B448, 2001.
32. Lin SL, Miller JD, Ying SY. Intronic MicroRNA (miRNA). J Biomed Biotechnol 2006: 26818, 2006.
33. Loos R, Thomis M, Maes HH, Beunen G, Claessens AL, Derom C, Legius E, Derom R, Vlietinck R. Gender-specific regional changes in genetic structure of muscularity in early adolescence. J Appl Physiol 82: 1802-1810, 1997.
34. 2+-ATPase. J Biol Chem 264: 7059-7065, 1989.
35. Marzetti E, Leeuwenburgh C. Skeletal muscle apoptosis, sarcopenia and frailty at old age. Exp Gerontol 41: 1234-1238, 2006.
36. Marziniak M, Hasselmann D, Tilgen W, Sommer C, Dillmann D. Influence of a mutation of the calcium ATPase 2 (SERCA 2) gene in patients with Darier's disease on the central and peripheral nervous system. Klinische Neurophysiologie 35, 2004.
37. Newgard CB, Brady MJ, O'Doherty RM, Saltiel AR. Organizing glucose disposal: emerging roles of the glycogen targeting subunits of protein phosphatase-1. Diabetes 49: 1967-1977, 2000.
38. Nielsen JN, Richter EA. Regulation of glycogen synthase in skeletal muscle during exercise. Acta Physiol Scand 178: 309-319, 2003.
39. Ozaki K, Ohnishi Y, Iida A, Sekine A, Yamada R, Tsunoda T, Sato H, Sato H, Hori M, Nakamura Y, Tanaka T. Functional SNPs in the lymphotoxin-α gene that are associated with susceptibility to myocardial infarction. Nat Genet 32: 650-654, 2002.
40. Periasamy M, Kalyanasundaram A. SERCA pump isoforms: their role in calcium transport and disease. Muscle Nerve 35: 430-442, 2007.
41. Phan HM, Alpert JS, Fain M. Frailty, inflammation, and cardiovascular disease: evidence of a connection. Am J Geriatr Cardiol 17: 101-107, 2008.
42. Phillips SM. Resistance exercise: good for more than just Grandma and Grandpa's muscles. Appl Physiol Nutr Metab 32: 1198-1205, 2007.
43. Purcell S, Cherny SS, Sham P. Genetic Power Calculator: design of linkage and association genetic mapping studies of complex traits. Bioinformatics 19: 149-150, 2003.
44. Silventoinen K, Magnusson PK, Tynelius P, Kaprio J, Rasmussen F. Heritability of body size and muscle strength in young adulthood: a study of one million Swedish men. Genet Epidemiol 32: 341-349, 2008.
45. Stephens JC, Schneider JA, Tanguay DA, Choi J, Acharya T, Stanley SE, Jiang R, Messer CJ, Chew A, Han JH, Duan J, Carr JL, Lee MS, Koshy B, Kumar AM, Zhang G, Newell WR, Windemuth A, Xu C, Kalbfleisch TS, Shaner SL, Arnold K, Schulz V, Drysdale CM, Nandabalan K, Judson RS, Ruano G, Vovis GF. Haplotype variation and linkage disequilibrium in 313 human genes. Science 293: 489-493, 2001.
46. Surinya KH, Cox TC, May BK. Identification and characterization of a conserved erythroid-specific enhancer located in intron 8 of the human 5-aminolevulinate synthase 2 gene. J Biol Chem 273: 16798-16809, 1998.
47. The International HapMap Consortium. The International HapMap Project. Nature 426: 789-796, 2003.
48. Thomis MA, De Mars G, Windelinckx A, Peeters MW, Huygens W, Aerssens J, Beunen GP. Genome-wide linkage scan for resistance to muscle fatigue. Scand J Med Sci Sports 21: 580-588, 2011.
49. Thomis MA, Van Leemputte M, Maes HH, Blimkie CJR, Claessens AL, Marchal G, Willems E, Vlietinck RF, Beunen GP. Multivariate genetic analysis of maximal isometric muscle force at different elbow angles. J Appl Physiol 82: 959-967, 1997.
50. Thomis MAI, Beunen GP, Van Leemputte M, Maes HH, Blimkie CJ, Claessens AL, Marchal G, Willems E, Vlietinck RF. Inheritance of static and dynamic arm strength and some of its determinants. Acta Physiol Scand 163: 59-71, 1998.
51. Tiainen K, Sipila S, Alen M, Heikkinen E, Kaprio J, Koskenvuo M, Tolvanen A, Pajala S, Rantanen T. Shared genetic and environmental effects on strength and power in older female twins. Med Sci Sports Exerc 37: 72-78, 2005.
52. Tiainen KM, Perola M, Kovanen VM, Sipila S, Tuononen KA, Rikalainen K, Kauppinen MA, Widen EI, Kaprio J, Rantanen T, Kujala UM. Genetics of maximal walking speed and skeletal muscle characteristics in older women. Twin Res Hum Genet 11: 321-334, 2008.
53. Tiainen K, Sipila S, Alen M, Heikkinen E, Kaprio J, Koskenvuo M, Tolvanen A, Pajala S, Rantanen T. Heritability of maximal isometric muscle strength in older female twins. J Appl Physiol 96: 173-180, 2004.
54. Tiret L, Poirier O, Nicaud V, Barbaux S, Herrmann SM, Perret C, Raoux S, Francomme C, Lebard G, Tregouet D, Cambien F. Heterogeneity of linkage disequilibrium in human genes has implications for association studies of common diseases. Hum Mol Genet 11: 419-429, 2002.
55. Tokuhiro S, Yamada R, Chang X, Suzuki A, Kochi Y, Sawada T, Suzuki M, Nagasaki M, Ohtsuki M, Ono M, Furukawa H, Nagashima M, Yoshino S, Mabuchi A, Sekine A, Saito S, Takahashi A, Tsunoda T, Nakamura Y, Yamamoto K. An intronic SNP in a RUNX1 binding site of SLC22A4, encoding an organic cation transporter, is associated with rheumatoid arthritis. Nat Genet 35: 341-348, 2003
56. Vincent B, De Bock K, Ramaekers M, Van den Eede E, Hespel P, Thomis MA. ACTN3 (R577X) genotype is associated with fiber type distribution. Physiol Genomics 32: 58-63, 2007.
57. Wigginton JE, Abecasis GR. PEDSTATS: descriptive statistics, graphics and quality assessment for gene mapping data. Bioinformatics 21: 3445-3447, 2005.
58. Wijndaele K, Duvigneaud N, Matton L, Duquet W, Thomis M, Beunen G, Lefevre J, Philippaerts RM. Muscular strength, aerobic fitness, and metabolic syndrome risk in Flemish adults. Med Sci Sports Exerc 39: 233-240, 2007.
59. Wilcox MA, Pugh EW, Zhang H, Zhong X, Levinson DF, Kennedy GC, Wijsman EM. Comparison of single-nucleotide polymorphisms and microsatellite markers for linkage analysis in the COGA and simulated data sets for Genetic Analysis Workshop 14: Presentation Groups 1, 2, and 3. Genet Epidemiol 29, Suppl 1: S7-S28, 2005.
60. Windelinckx A, De Mars G, Huygens WH, Peeters MW, Vincent B, Wijmenga C, Lambrechts D, Delecluse C, Roth SM, Metter EJ, Ferrucci L, Aerssens J, Vlietinck R, Beunen GP, Thomis MAI. Comprehensive fine mapping of chr12q12-14 and follow-up replication identify activin receptor 1B (ACVR1B) as a muscle strength gene. Eur J Hum Genet 19: 208-215, 2010.
61. Windelinckx A, Vlietinck R, Aerssens J, Beunen G, Thomis MA. Selection of genes and single nucleotide polymorphisms for fine mapping starting from a broad linkage region. Twin Res Hum Genet 10: 871-885, 2007.
62. Wolfe RR. The underappreciated role of muscle in health and disease. Am J Clin Nutr 84: 475-482, 2006.
63. Xu H, Gregory SG, Hauser ER, Stenger JE, Pericak-Vance MA, Vance JM, Zuchner S, Hauser MA. SNPselector: a web tool for selecting SNPs for genetic association studies. Bioinformatics 21: 4181-4186, 2005.
64. 2+-ATPase gene. J Biol Chem 265: 4670-4677, 1990.