Musclin, A Myokine Induced by Aerobic Exercise, Retards Muscle Atrophy During Cancer Cachexia in Mice.

PGC1α aerobic exercise cancer cachexia muscle atrophy muscle wasting musclin myokine

Journal

Cancers
ISSN: 2072-6694
Titre abrégé: Cancers (Basel)
Pays: Switzerland
ID NLM: 101526829

Informations de publication

Date de publication:
12 Oct 2019
Historique:
received: 07 06 2019
revised: 20 09 2019
accepted: 09 10 2019
entrez: 17 10 2019
pubmed: 17 10 2019
medline: 17 10 2019
Statut: epublish

Résumé

Physical activity improves the prognosis of cancer patients, partly by contrasting the associated muscle wasting (cachexia), through still unknown mechanisms. We asked whether aerobic exercise causes secretion by skeletal muscles of proteins (myokines) that may contrast cachexia. Media conditioned by peroxisome proliferator-activated receptor γ coactivator 1α (PGC1α)-expressing myotubes, reproducing some metabolic adaptations of aerobic exercise, as increased mitochondrial biogenesis and oxidative phosphorylation, restrained constitutively active Forkhead box-containing subfamily O3 (caFoxO3)-induced proteolysis. Microarray analysis identified amphiregulin (AREG), natriuretic peptide precursor B (NppB), musclin and fibroblast growth factor 18 (FGF18) as myokines highly induced by PGC1α. Notably, only musclin tended to be low in muscle of mice with a rare human renal carcinoma; it was reduced in plasma and in muscles of C26-bearing mice and in atrophying myotubes, where PGC1α expression is impaired. Therefore, we electroporated the Tibialis Anterior (TA) of C26-bearing mice with musclin or (its receptor) natriuretic peptide receptor 3 (Npr3)-encoding plasmids and found a preserved fiber area, as a result of restrained proteolysis. Musclin knockout (KO) mice lose more muscle tissue during growth of two distinct cachexia-causing tumors. Running protected C26-bearing mice from cachexia, not changing tumor growth, and rescued the C26-induced downregulation of musclin in muscles and plasma. Musclin expression did not change in overloaded plantaris of mice, recapitulating partially muscle adaptations to anaerobic exercise. Musclin might, therefore, be beneficial to cancer patients who cannot exercise and are at risk of cachexia and may help to explain how aerobic exercise alleviates cancer-induced muscle wasting.

Identifiants

pubmed: 31614775
pii: cancers11101541
doi: 10.3390/cancers11101541
pmc: PMC6826436
pii:
doi:

Types de publication

Journal Article

Langues

eng

Subventions

Organisme : BLRD VA
ID : I01 BX004840
Pays : United States
Organisme : Fondazione Cariplo
ID : 2014-1164
Organisme : Associazione Italiana per la Ricerca sul Cancro
ID : 11423

Références

Oncotarget. 2015 Feb 20;6(5):3043-54
pubmed: 25460504
Front Physiol. 2016 Oct 19;7:472
pubmed: 27807421
EMBO J. 2012 Aug 1;31(15):3334-50
pubmed: 22773186
Oncogene. 2016 Dec 1;35(48):6212-6222
pubmed: 27212031
Genome Biol. 2002 Jun 18;3(7):RESEARCH0034
pubmed: 12184808
Int J Cancer. 2010 Oct 1;127(7):1706-17
pubmed: 20039316
Lancet Oncol. 2011 May;12(5):489-95
pubmed: 21296615
Nature. 2012 Jan 11;481(7382):463-8
pubmed: 22237023
J Physiol. 2003 Feb 1;546(Pt 3):851-8
pubmed: 12563009
Aging Cell. 2018 Apr;17(2):
pubmed: 29427317
BMC Cancer. 2014 Dec 24;14:997
pubmed: 25539728
Proc Natl Acad Sci U S A. 2015 Dec 29;112(52):16042-7
pubmed: 26668395
Physiol Genomics. 2014 Apr 1;46(7):256-67
pubmed: 24520153
Front Physiol. 2019 Mar 29;10:287
pubmed: 30984014
Sci Rep. 2018 May 18;8(1):7876
pubmed: 29777200
Am J Physiol Endocrinol Metab. 2019 Jun 1;316(6):E1081-E1092
pubmed: 30964708
Sci Signal. 2011 Nov 29;4(201):ra80
pubmed: 22126963
Proc Natl Acad Sci U S A. 2006 Oct 31;103(44):16260-5
pubmed: 17053067
Nature. 1998 Dec 10;396(6711):584-7
pubmed: 9859994
Exerc Sport Sci Rev. 2018 Oct;46(4):247-253
pubmed: 30001273
Bioinformatics. 2006 Jul 1;22(13):1600-7
pubmed: 16606683
Nat Rev Drug Discov. 2016 Oct;15(10):719-29
pubmed: 27616294
J Surg Oncol. 1980;13(2):111-6
pubmed: 7359917
Cell. 1999 Mar 19;96(6):857-68
pubmed: 10102273
J Endocrinol. 2009 May;201(2):287-95
pubmed: 19244276
Int J Biochem Cell Biol. 2013 Oct;45(10):2191-9
pubmed: 23702032
Physiol Rep. 2015 Oct;3(10):null
pubmed: 26438733
Biochem Biophys Res Commun. 2002 Aug 16;296(2):350-4
pubmed: 12163024
J Cachexia Sarcopenia Muscle. 2013 Jun;4(2):111-24
pubmed: 23239116
Mol Cell Biol. 2004 Nov;24(21):9295-304
pubmed: 15485899
Nucleic Acids Res. 2015 Apr 20;43(7):e47
pubmed: 25605792
J Appl Physiol (1985). 2003 Nov;95(5):2171-9
pubmed: 12897032
J Appl Physiol (1985). 2001 May;90(5):1936-42
pubmed: 11299288
PLoS One. 2018 May 29;13(5):e0198089
pubmed: 29813127
Am J Physiol Gastrointest Liver Physiol. 2000 Jun;278(6):G974-80
pubmed: 10859228
Cell Metab. 2011 Feb 2;13(2):160-9
pubmed: 21284983
Life Sci. 2015 Mar 15;125:9-14
pubmed: 25500304
Med Sci Sports. 1975 Fall;7(3):185-98
pubmed: 128681
Am J Clin Nutr. 2011 Apr;93(4):884S-90
pubmed: 21289221
Ann Anat. 1995 May;177(3):285-9
pubmed: 7598225
FASEB J. 2005 May;19(7):786-8
pubmed: 15716393
Cell Metab. 2015 Jul 7;22(1):4-11
pubmed: 26073496
Curr Opin Genet Dev. 2008 Oct;18(5):426-34
pubmed: 18782618
Med Sci Sports Exerc. 2019 Jul;51(7):1387-1395
pubmed: 30724848
Mol Cell Biochem. 2019 Jun;456(1-2):15-27
pubmed: 30519782
J Biol Chem. 2007 Oct 12;282(41):30014-21
pubmed: 17702743
J Clin Invest. 2012 Dec;122(12):4675-9
pubmed: 23114600
Nat Rev Cancer. 2014 Nov;14(11):754-62
pubmed: 25291291
Cell Metab. 2016 Mar 8;23(3):554-62
pubmed: 26895752
J Cachexia Sarcopenia Muscle. 2015 Jun;6(2):115-24
pubmed: 26136187
Biochem Biophys Res Commun. 2007 Dec 14;364(2):358-65
pubmed: 17950246
J Cachexia Sarcopenia Muscle. 2012 Mar;3(1):37-43
pubmed: 22450815
J Muscle Res Cell Motil. 2003;24(2-3):113-9
pubmed: 14609022
Rev Assoc Med Bras (1992). 2017 Feb;63(2):164-172
pubmed: 28355378
J Biol Chem. 2004 May 7;279(19):19391-5
pubmed: 15044443
Cancer Genet Cytogenet. 2002 Dec;139(2):126-32
pubmed: 12550772
Genome Res. 2002 Jul;12(7):1121-6
pubmed: 12097350
Cell. 2004 Apr 30;117(3):399-412
pubmed: 15109499
Nat Commun. 2017 Nov 22;8(1):1707
pubmed: 29167426
Clin Biochem. 2017 Dec;50(18):1281-1288
pubmed: 28739222
Endocr Rev. 2003 Feb;24(1):78-90
pubmed: 12588810
Int J Oncol. 2006 Jun;28(6):1393-400
pubmed: 16685441
J Biol Chem. 2007 Dec 14;282(50):36454-62
pubmed: 17951249
J Biol Chem. 2002 Apr 5;277(14):11910-7
pubmed: 11809761
Horm Metab Res. 2006 Sep;38(9):614-6
pubmed: 16981146
Curr Opin Support Palliat Care. 2015 Dec;9(4):317-24
pubmed: 26509857
Nucleic Acids Res. 2000 Jan 1;28(1):27-30
pubmed: 10592173
J Biol Chem. 2003 Dec 12;278(50):50563-71
pubmed: 14523025
Endocr Rev. 2006 Feb;27(1):47-72
pubmed: 16291870
Mediators Inflamm. 2008;2008:109502
pubmed: 19148295
Circ Heart Fail. 2012 Jan;5(1):116-25
pubmed: 22135402
FEBS Lett. 2008 Nov 12;582(27):3805-10
pubmed: 18948104
Cell Metab. 2011 Jun 8;13(6):627-38
pubmed: 21641545
Am J Physiol Regul Integr Comp Physiol. 2011 Feb;300(2):R201-11
pubmed: 21148472
J Cachexia Sarcopenia Muscle. 2018 Apr;9(2):348-357
pubmed: 29464940
J Biol Chem. 2010 Jun 18;285(25):19460-71
pubmed: 20404331
Aging Cell. 2013 Dec;12(6):943-9
pubmed: 23802635
FEBS Lett. 1997 Jun 9;409(2):253-7
pubmed: 9202156
Diabetes. 2009 Dec;58(12):2880-92
pubmed: 19690065
Circ Res. 2018 Mar 2;122(5):742-751
pubmed: 29326144

Auteurs

Andrea D Re Cecconi (AD)

Department of Neurosciences, Mario Negri Institute for Pharmacological Research IRCCS, 20156 Milan, Italy. andrea.rececconi@marionegri.it.

Mara Forti (M)

Department of Neurosciences, Mario Negri Institute for Pharmacological Research IRCCS, 20156 Milan, Italy. mara.forti@guest.marionegri.it.

Michela Chiappa (M)

Department of Neurosciences, Mario Negri Institute for Pharmacological Research IRCCS, 20156 Milan, Italy. michela.chiappa@marionegri.it.

Zhiyong Zhu (Z)

Department of Internal Medicine, University of Iowa Carver College of Medicine, Iowa City, IA 52242, USA. zhiyong-zhu@uiowa.edu.
Fraternal Order of Eagles Diabetes Research Center, University of Iowa Carver College of Medicine, Iowa City, IA 52242, USA. zhiyong-zhu@uiowa.edu.
Department of Medicine, Medical Center, Department of Veterans Affairs, Iowa City, IA 52246, USA. zhiyong-zhu@uiowa.edu.

Leonid V Zingman (LV)

Department of Internal Medicine, University of Iowa Carver College of Medicine, Iowa City, IA 52242, USA. leonid-zingman@uiowa.edu.
Fraternal Order of Eagles Diabetes Research Center, University of Iowa Carver College of Medicine, Iowa City, IA 52242, USA. leonid-zingman@uiowa.edu.
Department of Medicine, Medical Center, Department of Veterans Affairs, Iowa City, IA 52246, USA. leonid-zingman@uiowa.edu.

Luigi Cervo (L)

Department of Neurosciences, Mario Negri Institute for Pharmacological Research IRCCS, 20156 Milan, Italy. luigi.cervo@marionegri.it.

Luca Beltrame (L)

Department of Oncology, Mario Negri Institute for Pharmacological Research IRCCS, 20156 Milan, Italy. luca.beltrame@marionegri.it.

Sergio Marchini (S)

Department of Oncology, Mario Negri Institute for Pharmacological Research IRCCS, 20156 Milan, Italy. sergio.marchini@marionegri.it.

Rosanna Piccirillo (R)

Department of Neurosciences, Mario Negri Institute for Pharmacological Research IRCCS, 20156 Milan, Italy. rosanna.piccirillo@marionegri.it.

Classifications MeSH