REGULAÇÃO GÊNICA DA VIA AMPK PELO EXERCÍCIO FÍSICO: REVISÃO SISTEMÁTICA E ANÁLISE <i>IN SILICO</i>

Pacheco, Christina; Santos, Luiz Henrique Pontes dos; Alves, Juliana Osório; Queiroz, Adriano Nogueira de; Soares, Paula Matias; Ceccatto, Vânia Marilande

doi:10.1590/1517-869220172304169935

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Revista Brasileira de Medicina do Esporte

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Sumário

Artigo de Revisão Sistemática • Rev Bras Med Esporte 23 (04) • Jul-Aug 2017 • https://doi.org/10.1590/1517-869220172304169935 copiar

REGULAÇÃO GÊNICA DA VIA AMPK PELO EXERCÍCIO FÍSICO: REVISÃO SISTEMÁTICA E ANÁLISE IN SILICO

AMPK PATHWAY GENE REGULATION BY PHYSICAL EXERCISE: SYSTEMATIC REVIEW AND IN SILICO ANALYSIS

REGULACIÓN GÉNICA DE LA VÍA AMPK POR EL EJERCICIO FÍSICO: REVISIÓN SISTEMÁTICA Y ANÁLISIS IN SILICO

Autoria SCIMAGO INSTITUTIONS RANKINGS

RESUMO

Introdução:

Novos estudos de regulação gênica do exercício físico por meio de técnicas pós-genômicas em ensaios de resistência (endurance) e força caracterizam a transcriptômica do exercício físico. Entre os genes afetados, destacamos a via da proteína quinase ativada por AMP (AMPK), cuja ativação ocorre durante o exercício como resultado das alterações dos níveis de fosfato energético da fibra muscular.

Objetivo:

Avaliar a via de sinalização da AMPK por revisão sistemática da expressão de genes e análise in silico.

Método:

Foi efetuada uma revisão sistemática para avaliar a regulação gênica da via de sinalização AMPK, caracterizando os genes estudados na literatura, as variações de regulação obtidas, na forma de fold change e tipos de exercício usados.

Resultados:

A via de sinalização AMPK mostrou 133 genes no repositório KEGG (Kyoto Encyclopedia of Genes and Genomes), os quais foram confrontados com a revisão sistemática da literatura, totalizando 65 genes. Dezessete genes apresentaram UR e 24 mostraram DR com relação ao seu respectivo controle. Além destes, 20 genes estavam presentes nos trabalhos, apresentando tanto UR e DR e quatro genes não apresentaram dados de regulação. Verificou-se regulação específica em função do tipo de exercício efetuado.

Discussão:

Dos 133 genes da via AMPK, 48,8% foram amostrados nos trabalhos revisados, indicando que uma parte significativa da via é regulada pelo exercício. O estudo apresentou a regulação gênica básica de dois mecanismos para a recuperação energética, a biogênese mitocondrial e o bloqueio da gliconeogênese.

Conclusão:

Este trabalho mostrou que o exercício atua ativamente na via de sinalização da AMPK, na importância da regulação via PGC-1α e no papel de outros genes, regulando a expressão de mais da metade dos genes amostrados.

Descritores:
AMP cíclico; transcrição genética; exercício

Sociedade Brasileira de Medicina do Exercício e do Esporte Av. Brigadeiro Luís Antônio, 278, 6º and., 01318-901 São Paulo SP, Tel.: +55 11 3106-7544, Fax: +55 11 3106-8611 - São Paulo - SP - Brazil
E-mail: atharbme@uol.com.br

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[1] Correspondência: Vânia Marilande Ceccatto Universidade Estadual do Ceará, Instituto Superior de Ciências Biomédicas, Laboratório de Bioquímica e Expressão Gênica. Rua Dr. Silas Munguba, 1700, Campus do Itaperi, Fortaleza, CE, Brasil. 60.714 903. vania.ceccatto@uece.br

Gene (Símbolo original)	Nome (Nome original)	Fold Change	Tipo de exercício	Referência
PPARGC1A	Peroxisome proliferator-activated receptor gamma, coactivator 1 alpha	10,0 -1,01	E R	^{Bray et al.15 , 2009}15 - Bray MS, Hagberg JM, Pérusse L, Rankinen T, Roth SM, Wolfarth B, et al. The human gene map for performance and health-related fitness phenotypes: the 2006-2007 update. Med Sci Sports Exerc. 2009;41(1):35-73.; ^{Psilander et al.16 , 2010}16 - Psilander N, Wang L, Westergren J, Tonkonogi M, Sahlin K. Mitochondrial gene expression in elite cyclists: effects of high-intensity interval exercise. Eur J Appl Physiol. 2010;110(3):597-606.; ^{Pilegaard et al.17, 2003}17 - Pilegaard H, Saltin B, Neufer PD. Exercise induces transient transcriptional activation of the PGC-1a gene in human skeletal muscle. J Physiol. 2003;546(Pt 3):851-8.; ^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.; ^{Egan e Zierath18, 2013}18 - Egan B, Zierath JR. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 2013;17(2):162-84.; ^{Gibala et al.19, 2009}19 - Gibala MJ, McGee SL, Garnham AP, Howlett KF, Snow RJ, Hargreaves M. Brief intense interval exercise activates AMPK and p38 MAPK signaling and increases the expression of PGC-1alpha in human skeletal muscle. J Appl Physiol (1985). 2009;106(3):929-34.; ^{Popov et al.20, 2014}20 - Popov D, Zinovkin R, Karger E, Tarasova O, Vinogradova O. Effects of continuous and intermittent aerobic exercise upon mRNA expression of metabolic genes in human skeletal muscle. J Sports Med Phys Fitness. 2014;54(3):362-9.
SCD	Stearoyl-CoAdesaturase (delta-9-desaturase)	7,20	E	^{Timmons et al.21, 2010}21 - Timmons JA, Knudsen S, Rankinen T, Koch LG, Sarzynski M, Jensen T, et al. Using molecular classification to predict gains in maximal aerobic capacity following endurance exercise training in humans. J Appl Physiol (1985). 2010;108(6):1487-96.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
PRKAG2	Protein kinase, AMP-activated, gamma 2 non-catalytic subunit	4,79	E R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
CCND1	Cyclin D1	3,80	E R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.; ^{Timmons et al.21, 2010}21 - Timmons JA, Knudsen S, Rankinen T, Koch LG, Sarzynski M, Jensen T, et al. Using molecular classification to predict gains in maximal aerobic capacity following endurance exercise training in humans. J Appl Physiol (1985). 2010;108(6):1487-96.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
IRS2	Insulin receptor substrate 2	3,41 -1,93	E R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
PDPK1	3-Phosphoinositide dependentproteinkinase 1	-2,27	E R	^{Stepto et al.23, 2009}23 - Stepto NK, Coffey VG, Carey, et al. Global gene expression in skeletal muscle from well-trained strength and endurance athletes. Med Sci Sports Exerc. 2009;41(3):546-5.
PFKL	Phosphofructokinase, liver	2,20	E	^{Timmons et al.21, 2010}21 - Timmons JA, Knudsen S, Rankinen T, Koch LG, Sarzynski M, Jensen T, et al. Using molecular classification to predict gains in maximal aerobic capacity following endurance exercise training in humans. J Appl Physiol (1985). 2010;108(6):1487-96.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
RAB11B	RAB11B, member RAS oncogene family	1,80	E	^{Timmons et al.21, 2010}21 - Timmons JA, Knudsen S, Rankinen T, Koch LG, Sarzynski M, Jensen T, et al. Using molecular classification to predict gains in maximal aerobic capacity following endurance exercise training in humans. J Appl Physiol (1985). 2010;108(6):1487-96.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
FOXO1	Forkhead box O1	1,80	E R	^{Popov et al.20, 2014}20 - Popov D, Zinovkin R, Karger E, Tarasova O, Vinogradova O. Effects of continuous and intermittent aerobic exercise upon mRNA expression of metabolic genes in human skeletal muscle. J Sports Med Phys Fitness. 2014;54(3):362-9.; ^{Egan e Zierath18, 2013}18 - Egan B, Zierath JR. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 2013;17(2):162-84.
LIPE	Lipase, hormone-sensitive	1,7 -1,12	E R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.; ^{Timmons et al.21, 2010}21 - Timmons JA, Knudsen S, Rankinen T, Koch LG, Sarzynski M, Jensen T, et al. Using molecular classification to predict gains in maximal aerobic capacity following endurance exercise training in humans. J Appl Physiol (1985). 2010;108(6):1487-96.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
MLYCD	Malonyl-CoAdecarboxylase	1,65	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
EIF4EBP1	Eukaryotic translation initiation factor 4E binding protein 1	-1,52	R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.;
PPARG	Peroxisomeproliferator-activated receptor gamma, coactivator 1 alpha	1,50	E R	^{Bray et al.15, 2009}15 - Bray MS, Hagberg JM, Pérusse L, Rankinen T, Roth SM, Wolfarth B, et al. The human gene map for performance and health-related fitness phenotypes: the 2006-2007 update. Med Sci Sports Exerc. 2009;41(1):35-73.; ^{Egan e Zierath18, 2013}18 - Egan B, Zierath JR. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 2013;17(2):162-84.; ^{Ruchat et al.24, 2009}24 - Ruchat SM, Rankinen T, Weisnagel SJ, Rice T, Rao DC, Bergman RN, et al. Improvements in glucose homeostasis in response to regular exercise are influenced by the PPARG Pro12Ala variant: results from the HERITAGE Family Study. Diabetologia. 2009;53(4):679-9.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
CD36	CD36 molecule (thrombospondin receptor)	1,50 -1,15	E	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.; ^{Timmons et al.21, 2010}21 - Timmons JA, Knudsen S, Rankinen T, Koch LG, Sarzynski M, Jensen T, et al. Using molecular classification to predict gains in maximal aerobic capacity following endurance exercise training in humans. J Appl Physiol (1985). 2010;108(6):1487-96.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
AKT3	V-akt murine thymoma viral oncogene homolog 3	1,50	R	^{Timmons et al.21, 2010}21 - Timmons JA, Knudsen S, Rankinen T, Koch LG, Sarzynski M, Jensen T, et al. Using molecular classification to predict gains in maximal aerobic capacity following endurance exercise training in humans. J Appl Physiol (1985). 2010;108(6):1487-96.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
CPT1B	Carnitinepalmitoyltransferase 1B (muscle)	-1,49	R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.
CPT1A	Carnitine palmitoyltransferase 1A (liver)	1,49	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
PRKAG3	Protein kinase, AMP-activated, gamma 3 non-catalytic subunit	-1,47	E	^{Timmons et al.21, 2010}21 - Timmons JA, Knudsen S, Rankinen T, Koch LG, Sarzynski M, Jensen T, et al. Using molecular classification to predict gains in maximal aerobic capacity following endurance exercise training in humans. J Appl Physiol (1985). 2010;108(6):1487-96.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
CREB3L1	cAMP responsive element binding protein 3-like 1	1,41	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
IGF1	Insulin-like growth factor 1 (somatomedin C)	-1,30 2,50	R	^{Bray et al.15, 2009}15 - Bray MS, Hagberg JM, Pérusse L, Rankinen T, Roth SM, Wolfarth B, et al. The human gene map for performance and health-related fitness phenotypes: the 2006-2007 update. Med Sci Sports Exerc. 2009;41(1):35-73.; ^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.; ^{Timmons et al.21, 2010}21 - Timmons JA, Knudsen S, Rankinen T, Koch LG, Sarzynski M, Jensen T, et al. Using molecular classification to predict gains in maximal aerobic capacity following endurance exercise training in humans. J Appl Physiol (1985). 2010;108(6):1487-96.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
PRKAA2	protein kinase, AMP-activated, alpha 2 catalytic subunit	-1,29	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
TSC1	Tuberoussclerosis 1	-1,25	R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
RPS6KB1	Ribosomalprotein S6 kinase, 70kDa, polypeptide 1	-1,25	R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
PFKFB3	6-phosphofructo-2-kinase/fructose-2,6-biphosphatase 3	1,25 -6,14	R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
CAB39	Calciumbindingprotein 39-like	-1,24	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
IGF1R	Insulin-like growth factor 1 receptor	-1,24	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
GYS1	Glycogensynthase 1 (muscle)	1,24 -1,17	R	^{Bray et al.15, 2009}15 - Bray MS, Hagberg JM, Pérusse L, Rankinen T, Roth SM, Wolfarth B, et al. The human gene map for performance and health-related fitness phenotypes: the 2006-2007 update. Med Sci Sports Exerc. 2009;41(1):35-73.; ^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.;
PIK3CD	Phosphatidylinositol-4,5-bisphosphate 3-kinase, catalytic subunit delta	1,24	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
PFKFB2	6-phosphofructo-2-kinase/fructose-2,6-biphosphatase 2	1,22	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
PPP2R3A	Protein phosphatase 2, regulatory subunit B’’, alpha	-1,21	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
FOXO3	Forkhead box O3	1,21 -1,78	R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.; ^{Egan e Zierath18, 2013}18 - Egan B, Zierath JR. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 2013;17(2):162-84.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
CAB39L	Calciumbindingprotein 39-like	-1,20	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
PFKM	Phosphofructokinase, muscle	1,18 -1,12	R	^{Bray et al.15, 2009}15 - Bray MS, Hagberg JM, Pérusse L, Rankinen T, Roth SM, Wolfarth B, et al. The human gene map for performance and health-related fitness phenotypes: the 2006-2007 update. Med Sci Sports Exerc. 2009;41(1):35-73.; ^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.
RHEB	Ras homolog enriched in brain	1,18 -1,07	R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
MAP3K7	Mitogen-activated protein kinase kinasekinase 7	-1,17	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
CAMK2	Calcium/calmodulin-dependent protein kinase kinase 2, beta	1,17	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
PIK3CA	Phosphatidylinositol-4,5-bisphosphate 3-kinase, catalytic subunit alpha	-1,16	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
Gene (Símbolo original)	Nome (Nome original)	Fold Change	Tipo de exercício	Referência
PFKP	Phosphofructokinase, platelet	1,16	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
TBC1D1	TBC1 domain family, member 10A	-1,15	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
PIK3CB	Phosphatidylinositol-4,5-bisphosphate 3-kinase, catalytic subunit beta	-1,14	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
PPP2R3B	Protein phosphatase 2, regulatory subunit B’’, beta	-1,13	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
PPP2R5A	Protein phosphatase 2, regulatory subunit B’, alpha	-1,13	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
ACACA	Acetyl-CoA carboxylase alpha	1,13	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
INSR	Insulin receptor	-1,12	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
RPS6KB2	Ribosomalprotein S6 kinase, 70kDa, polypeptide 2	-1,12	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
ACACB	Acetyl-CoA carboxylase beta	1,12	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
PRKAB2	Protein kinase, AMP-activated, beta 2 non-catalytic subunit	-1,11	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
ULK1	unc-51 like autophagy activating kinase 1	-1,11	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
RAB2A	RAB2A, member RAS oncogene family	-1,10	E	^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
TSC2	TSC22 domainfamily, member 3	1,10 -1,12	E	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.
SLC2A4	Solutecarrierfamily 2	1,08 -1,34	R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.
IRS1	Insulin receptor substrate 1	1,07 -1,54	R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.
EEF2K	Eukaryoticelongation factor-2 kinase	1,05 -1,55	E R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.; ^{Timmons et al.21, 2010}21 - Timmons JA, Knudsen S, Rankinen T, Koch LG, Sarzynski M, Jensen T, et al. Using molecular classification to predict gains in maximal aerobic capacity following endurance exercise training in humans. J Appl Physiol (1985). 2010;108(6):1487-96.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
mTOR	Late endosomal/lysosomal adaptor, MAPK and MTOR activator 5	1,05 -1,09	E	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.
SREBF1	Sterol regulatory element binding transcription factor 1	1,03 -1,49	R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.
AKT1	v-akt murine thymoma viral oncogene homolog 1	1,01 -1,45	E R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.; ^{Timmons et al.21, 2010}21 - Timmons JA, Knudsen S, Rankinen T, Koch LG, Sarzynski M, Jensen T, et al. Using molecular classification to predict gains in maximal aerobic capacity following endurance exercise training in humans. J Appl Physiol (1985). 2010;108(6):1487-96.; ^{Lindholm et al.22, 2014}22 - Lindholm ME, Marabita F, Gomez-Cabrero D, Rundqvist H, Ekström TJ, Tegnér J, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014;9(12):1557-69.
AKT1S1	AKT1 substrate 1 (proline-rich)	1,01 -1,45	R	^{Liu et al.9, 2010}9 - Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.;
CFTR	Cysticfibrosistransmembraneconductanceregulator	*	-	^{Bray et al.15, 2009}15 - Bray MS, Hagberg JM, Pérusse L, Rankinen T, Roth SM, Wolfarth B, et al. The human gene map for performance and health-related fitness phenotypes: the 2006-2007 update. Med Sci Sports Exerc. 2009;41(1):35-73.
LEP	Leptin	*	E R	^{Bray et al.15, 2009}15 - Bray MS, Hagberg JM, Pérusse L, Rankinen T, Roth SM, Wolfarth B, et al. The human gene map for performance and health-related fitness phenotypes: the 2006-2007 update. Med Sci Sports Exerc. 2009;41(1):35-73.; ^{Walsh et al.25, 2012}25 - Walsh S, Haddad CJ, Kostek MA, Angelopoulos TJ, Clarkson PM, Gordon PM, et al. Leptin and leptin receptor genetic variants associate with habitual physical activity and the arm body composition response to resistance training. Gene. 2012;510(1):66-70.; ^{Golbidi e Laher26, 2014}26 - Golbidi S, Laher I. Exercise induced adipokine changes and the metabolic syndrome. J Diabetes Res. 2014;2014:726861.; ^{Moran et al.27, 2011}27 - Moran CN, Barwell ND, Malkova D, Cleland SJ, McPhee I, Packard CJ, et al. Effects of diabetes family history and exercise training on the expression of adiponectin and leptin and their receptors. Metabolism. 2011;60(2):206-4.. ^{Kraemer e Castracane 28, 2007}28 - Kraemer, RR, Castracane VD. Exercise and humoral mediators of peripheral energy balance: ghrelin and adiponectin. Exp Biol Med (Maywood). 2007;232(2):184-94.
LEPR	Leptin receptor	*	R	^{Bray et al.15, 2009}15 - Bray MS, Hagberg JM, Pérusse L, Rankinen T, Roth SM, Wolfarth B, et al. The human gene map for performance and health-related fitness phenotypes: the 2006-2007 update. Med Sci Sports Exerc. 2009;41(1):35-73.; ^{De Moor et al. 29, 2009}29 - De Moor MHM, Liu YJ, Boomsma DI, Li J, Hamilton JJ, Hottenga JJ, et al. Genome-wide Association Study of Exercise Behavior in Dutch and American Adults. MedSci Sports Exerc. 2009;41(10):1887-95.; ^{Walsh et al.25, 2012}25 - Walsh S, Haddad CJ, Kostek MA, Angelopoulos TJ, Clarkson PM, Gordon PM, et al. Leptin and leptin receptor genetic variants associate with habitual physical activity and the arm body composition response to resistance training. Gene. 2012;510(1):66-70.
ADIPOR1	Adiponectin receptor 1	*	-	^{Bray et al.15, 2009}15 - Bray MS, Hagberg JM, Pérusse L, Rankinen T, Roth SM, Wolfarth B, et al. The human gene map for performance and health-related fitness phenotypes: the 2006-2007 update. Med Sci Sports Exerc. 2009;41(1):35-73.
CREB1	cAMP responsive element binding protein 1	*	E	^{Egan e Zierath18, 2013}18 - Egan B, Zierath JR. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 2013;17(2):162-84.;
SIRT1	Sirtuin 1	*	E	^{Egan e Zierath18, 2013}18 - Egan B, Zierath JR. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 2013;17(2):162-84.;
PRKAA1	Protein kinase, AMP-activated, alpha 1 catalytic subunit	*	E	^{Gibala et al.19, 2009}19 - Gibala MJ, McGee SL, Garnham AP, Howlett KF, Snow RJ, Hargreaves M. Brief intense interval exercise activates AMPK and p38 MAPK signaling and increases the expression of PGC-1alpha in human skeletal muscle. J Appl Physiol (1985). 2009;106(3):929-34.
http://www.ensembl.org/Homo_sapiens/Gene/Summary?db=core;g=ENSG00000145675	Phosphoinositide-3-kinase, regulatorysubunit 1	*	R	^{Radom-Aizik et al. 30, 2013}30 - Radom-Aizik S, Zaldivar F, Haddad F, Cooper DM. Impact of brief exercise on peripheral blood NK cell gene and microRNA expression in young adults. J Appl Physiol (1985). 2013;114(5):628-36.