Acute and Chronic Increases of Circulating FSTL1 Normalize Energy Substrate Metabolism in Pacing-Induced Heart Failure

FSTL1 (follistatin-like protein 1) is an emerging cardiokine/myokine that is upregulated in heart failure (HF) and is found to be cardioprotective in animal models of cardiac injury. We tested the hypothesis that circulating FSTL1 can affect cardiac function and metabolism under baseline physiologic...

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Published inCirculation. Heart failure Vol. 11; no. 1; p. e004486
Main Authors Seki, Mitsuru, Powers, Jeffery C., Maruyama, Sonomi, Zuriaga, Maria A., Wu, Chia-Ling, Kurishima, Clara, Kim, Lydia, Johnson, Jesse, Poidomani, Anthony, Wang, Tao, Muñoz, Eric, Rajan, Sudarsan, Park, Joon Y., Walsh, Kenneth, Recchia, Fabio A.
Format Journal Article
LanguageEnglish
Published United States 01.01.2018
Subjects
heart failure
glucose
myocardium
animals
heart
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Abstract FSTL1 (follistatin-like protein 1) is an emerging cardiokine/myokine that is upregulated in heart failure (HF) and is found to be cardioprotective in animal models of cardiac injury. We tested the hypothesis that circulating FSTL1 can affect cardiac function and metabolism under baseline physiological conditions and in HF. FSTL1 was acutely (10 minutes) or chronically (2 weeks) infused to attain clinically relevant blood levels in conscious dogs with cardiac tachypacing-induced HF. Dogs with no cardiac pacing and FSTL1 infusion served as control. H-oleate and C-glucose were infused to track the metabolic fate of free fatty acids and glucose. Cardiac uptake of lactate and ketone bodies and systemic respiratory quotient were also measured. HF caused a shift from prevalent cardiac and systemic fat to carbohydrate oxidation. Although acute FSTL1 administration caused minimal hemodynamic changes at baseline, in HF dogs it enhanced cardiac oxygen consumption and transiently reversed the changes in free fatty acid and glucose oxidation and systemic respiratory quotient. In HF, chronic FSTL1 infusion stably normalized cardiac free fatty acid, glucose, ketone body consumption, and systemic respiratory quotient, while moderately improving diastolic and contractile function. Consistently, FSTL1 prevented the downregulation of medium-chain acyl-CoA dehydrogenase-a representative enzyme of the free fatty acid oxidation pathway. Complementary in vitro experiments in primary cardiac and skeletal muscle myocytes showed that FSTL1 stimulated oxygen consumption through AMPK (AMP-activated kinase) activation. These findings support a novel function for FSTL1 and provide the first direct evidence that a circulating cardiokine/myokine can alter myocardial and systemic energy substrate metabolism, in vivo.
AbstractList FSTL1 (follistatin-like protein 1) is an emerging cardiokine/myokine that is upregulated in heart failure (HF) and is found to be cardioprotective in animal models of cardiac injury. We tested the hypothesis that circulating FSTL1 can affect cardiac function and metabolism under baseline physiological conditions and in HF.BACKGROUNDFSTL1 (follistatin-like protein 1) is an emerging cardiokine/myokine that is upregulated in heart failure (HF) and is found to be cardioprotective in animal models of cardiac injury. We tested the hypothesis that circulating FSTL1 can affect cardiac function and metabolism under baseline physiological conditions and in HF.FSTL1 was acutely (10 minutes) or chronically (2 weeks) infused to attain clinically relevant blood levels in conscious dogs with cardiac tachypacing-induced HF. Dogs with no cardiac pacing and FSTL1 infusion served as control. 3H-oleate and 14C-glucose were infused to track the metabolic fate of free fatty acids and glucose. Cardiac uptake of lactate and ketone bodies and systemic respiratory quotient were also measured. HF caused a shift from prevalent cardiac and systemic fat to carbohydrate oxidation. Although acute FSTL1 administration caused minimal hemodynamic changes at baseline, in HF dogs it enhanced cardiac oxygen consumption and transiently reversed the changes in free fatty acid and glucose oxidation and systemic respiratory quotient. In HF, chronic FSTL1 infusion stably normalized cardiac free fatty acid, glucose, ketone body consumption, and systemic respiratory quotient, while moderately improving diastolic and contractile function. Consistently, FSTL1 prevented the downregulation of medium-chain acyl-CoA dehydrogenase-a representative enzyme of the free fatty acid oxidation pathway. Complementary in vitro experiments in primary cardiac and skeletal muscle myocytes showed that FSTL1 stimulated oxygen consumption through AMPK (AMP-activated kinase) activation.METHODS AND RESULTSFSTL1 was acutely (10 minutes) or chronically (2 weeks) infused to attain clinically relevant blood levels in conscious dogs with cardiac tachypacing-induced HF. Dogs with no cardiac pacing and FSTL1 infusion served as control. 3H-oleate and 14C-glucose were infused to track the metabolic fate of free fatty acids and glucose. Cardiac uptake of lactate and ketone bodies and systemic respiratory quotient were also measured. HF caused a shift from prevalent cardiac and systemic fat to carbohydrate oxidation. Although acute FSTL1 administration caused minimal hemodynamic changes at baseline, in HF dogs it enhanced cardiac oxygen consumption and transiently reversed the changes in free fatty acid and glucose oxidation and systemic respiratory quotient. In HF, chronic FSTL1 infusion stably normalized cardiac free fatty acid, glucose, ketone body consumption, and systemic respiratory quotient, while moderately improving diastolic and contractile function. Consistently, FSTL1 prevented the downregulation of medium-chain acyl-CoA dehydrogenase-a representative enzyme of the free fatty acid oxidation pathway. Complementary in vitro experiments in primary cardiac and skeletal muscle myocytes showed that FSTL1 stimulated oxygen consumption through AMPK (AMP-activated kinase) activation.These findings support a novel function for FSTL1 and provide the first direct evidence that a circulating cardiokine/myokine can alter myocardial and systemic energy substrate metabolism, in vivo.CONCLUSIONSThese findings support a novel function for FSTL1 and provide the first direct evidence that a circulating cardiokine/myokine can alter myocardial and systemic energy substrate metabolism, in vivo.
FSTL1 (follistatin-like protein 1) is an emerging cardiokine/myokine that is upregulated in heart failure (HF) and is found to be cardioprotective in animal models of cardiac injury. We tested the hypothesis that circulating FSTL1 can affect cardiac function and metabolism under baseline physiological conditions and in HF. FSTL1 was acutely (10 minutes) or chronically (2 weeks) infused to attain clinically relevant blood levels in conscious dogs with cardiac tachypacing-induced HF. Dogs with no cardiac pacing and FSTL1 infusion served as control. H-oleate and C-glucose were infused to track the metabolic fate of free fatty acids and glucose. Cardiac uptake of lactate and ketone bodies and systemic respiratory quotient were also measured. HF caused a shift from prevalent cardiac and systemic fat to carbohydrate oxidation. Although acute FSTL1 administration caused minimal hemodynamic changes at baseline, in HF dogs it enhanced cardiac oxygen consumption and transiently reversed the changes in free fatty acid and glucose oxidation and systemic respiratory quotient. In HF, chronic FSTL1 infusion stably normalized cardiac free fatty acid, glucose, ketone body consumption, and systemic respiratory quotient, while moderately improving diastolic and contractile function. Consistently, FSTL1 prevented the downregulation of medium-chain acyl-CoA dehydrogenase-a representative enzyme of the free fatty acid oxidation pathway. Complementary in vitro experiments in primary cardiac and skeletal muscle myocytes showed that FSTL1 stimulated oxygen consumption through AMPK (AMP-activated kinase) activation. These findings support a novel function for FSTL1 and provide the first direct evidence that a circulating cardiokine/myokine can alter myocardial and systemic energy substrate metabolism, in vivo.
Author Zuriaga, Maria A.
Recchia, Fabio A.
Kim, Lydia
Maruyama, Sonomi
Park, Joon Y.
Wang, Tao
Seki, Mitsuru
Kurishima, Clara
Poidomani, Anthony
Walsh, Kenneth
Muñoz, Eric
Rajan, Sudarsan
Johnson, Jesse
Powers, Jeffery C.
Wu, Chia-Ling
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Cites_doi 10.1161/CIRCHEARTFAILURE.114.001167
10.1161/CIRCULATIONAHA.115.017355
10.1023/A:1026070911202
10.1093/cvr/cvu105
10.1038/nature15372
10.1074/jbc.M113.533851
10.1161/CIRCRESAHA.111.255505
10.1161/CIRCULATIONAHA.115.017545
10.1074/jbc.M109.069468
10.1373/clinchem.2012.182816
10.1074/jbc.M803440200
10.1681/ASN.2014020210
10.1161/01.CIR.94.11.2837
10.1161/CIRCULATIONAHA.108.798561
10.1161/CIRCRESAHA.117.309633
10.1038/nrendo.2012.49
10.1161/RES.0000000000000097
10.15252/emmm.201506151
10.1073/pnas.0500768102
10.1161/01.RES.83.10.969
10.1073/pnas.1108559108
10.1161/01.cir.0000023531.22727.c1
10.1161/CIRCULATIONAHA.108.767673
10.1161/CIRCULATIONAHA.112.150656
10.1016/j.molmed.2010.12.003
10.1016/j.jacc.2015.04.071
10.1253/circj.CJ-08-0961
10.1016/j.jacbts.2016.04.002
10.1056/NEJMoa1214091
10.1152/ajpendo.2002.282.1.E197
10.1161/CIRCULATIONAHA.112.115089
10.1161/CIRCHEARTFAILURE.110.960625
10.3892/mmr_00000281
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PublicationTitle Circulation. Heart failure
PublicationTitleAlternate Circ Heart Fail
PublicationYear 2018
References e_1_3_3_17_2
e_1_3_3_16_2
e_1_3_3_19_2
e_1_3_3_18_2
e_1_3_3_13_2
e_1_3_3_12_2
e_1_3_3_15_2
e_1_3_3_34_2
e_1_3_3_14_2
e_1_3_3_32_2
e_1_3_3_33_2
e_1_3_3_11_2
e_1_3_3_30_2
e_1_3_3_10_2
e_1_3_3_31_2
e_1_3_3_6_2
e_1_3_3_5_2
e_1_3_3_8_2
e_1_3_3_7_2
e_1_3_3_28_2
e_1_3_3_9_2
e_1_3_3_27_2
e_1_3_3_29_2
e_1_3_3_24_2
e_1_3_3_23_2
e_1_3_3_26_2
e_1_3_3_25_2
e_1_3_3_2_2
e_1_3_3_20_2
e_1_3_3_4_2
e_1_3_3_22_2
e_1_3_3_3_2
e_1_3_3_21_2
References_xml – ident: e_1_3_3_16_2
  doi: 10.1161/CIRCHEARTFAILURE.114.001167
– ident: e_1_3_3_27_2
  doi: 10.1161/CIRCULATIONAHA.115.017355
– ident: e_1_3_3_2_2
  doi: 10.1023/A:1026070911202
– ident: e_1_3_3_33_2
  doi: 10.1093/cvr/cvu105
– ident: e_1_3_3_11_2
  doi: 10.1038/nature15372
– ident: e_1_3_3_25_2
  doi: 10.1074/jbc.M113.533851
– ident: e_1_3_3_15_2
  doi: 10.1161/CIRCRESAHA.111.255505
– ident: e_1_3_3_28_2
  doi: 10.1161/CIRCULATIONAHA.115.017545
– ident: e_1_3_3_29_2
  doi: 10.1074/jbc.M109.069468
– ident: e_1_3_3_34_2
  doi: 10.1373/clinchem.2012.182816
– ident: e_1_3_3_8_2
  doi: 10.1074/jbc.M803440200
– ident: e_1_3_3_32_2
  doi: 10.1681/ASN.2014020210
– ident: e_1_3_3_30_2
  doi: 10.1161/01.CIR.94.11.2837
– ident: e_1_3_3_26_2
  doi: 10.1161/CIRCULATIONAHA.108.798561
– ident: e_1_3_3_31_2
  doi: 10.1161/CIRCRESAHA.117.309633
– ident: e_1_3_3_4_2
  doi: 10.1038/nrendo.2012.49
– ident: e_1_3_3_19_2
  doi: 10.1161/RES.0000000000000097
– ident: e_1_3_3_12_2
  doi: 10.15252/emmm.201506151
– ident: e_1_3_3_22_2
  doi: 10.1073/pnas.0500768102
– ident: e_1_3_3_20_2
  doi: 10.1161/01.RES.83.10.969
– ident: e_1_3_3_10_2
  doi: 10.1073/pnas.1108559108
– ident: e_1_3_3_21_2
  doi: 10.1161/01.cir.0000023531.22727.c1
– ident: e_1_3_3_7_2
  doi: 10.1161/CIRCULATIONAHA.108.767673
– ident: e_1_3_3_5_2
  doi: 10.1161/CIRCULATIONAHA.112.150656
– ident: e_1_3_3_6_2
  doi: 10.1016/j.molmed.2010.12.003
– ident: e_1_3_3_17_2
  doi: 10.1016/j.jacc.2015.04.071
– ident: e_1_3_3_3_2
  doi: 10.1253/circj.CJ-08-0961
– ident: e_1_3_3_14_2
  doi: 10.1016/j.jacbts.2016.04.002
– ident: e_1_3_3_24_2
  doi: 10.1056/NEJMoa1214091
– ident: e_1_3_3_18_2
  doi: 10.1152/ajpendo.2002.282.1.E197
– ident: e_1_3_3_9_2
  doi: 10.1161/CIRCULATIONAHA.112.115089
– ident: e_1_3_3_13_2
  doi: 10.1161/CIRCHEARTFAILURE.110.960625
– ident: e_1_3_3_23_2
  doi: 10.3892/mmr_00000281
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Snippet FSTL1 (follistatin-like protein 1) is an emerging cardiokine/myokine that is upregulated in heart failure (HF) and is found to be cardioprotective in animal...
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Title Acute and Chronic Increases of Circulating FSTL1 Normalize Energy Substrate Metabolism in Pacing-Induced Heart Failure
URI https://www.ncbi.nlm.nih.gov/pubmed/29317401
https://www.proquest.com/docview/1989569991
Volume 11
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