Arginine ingestion inhibits phagocyte invasion in eccentrically contracted rat fast-twitch muscle.
Inflammation
Muscle damage
Nitric oxide
Nitric oxide synthase
Journal
Journal of muscle research and cell motility
ISSN: 1573-2657
Titre abrégé: J Muscle Res Cell Motil
Pays: Netherlands
ID NLM: 8006298
Informations de publication
Date de publication:
18 Apr 2024
18 Apr 2024
Historique:
received:
31
01
2024
accepted:
29
03
2024
medline:
18
4
2024
pubmed:
18
4
2024
entrez:
18
4
2024
Statut:
aheadofprint
Résumé
Eccentric contraction (ECC) has been shown to induce leukocyte invasion into skeletal muscle, resulting in muscle inflammation. This study aimed to investigate whether prior ingestion of L-arginine (ARG), a nitric oxide precursor, inhibits ECC-induced macrophage invasion. Male Wistar rats received ARG in water for 7 days, beginning 3 days prior to ECC. ECCs were induced in the anterior crural muscles for 200 cycles. Three days later, the tibialis anterior and extensor digitorum longus muscles were excised for biochemical analysis and force measurement, respectively. ARG ingestion increased nitrite and nitrate levels in plasma and muscle, inhibiting force depression and reducing CD68 content in muscles subjected to ECC. ARG ingestion also ameliorated an ECC-induced increase in protein nitration, although neither ARG ingestion nor ECC induction affected protein carbonyl levels. The present results suggest that ingestion of ARG or ARG-rich foods may alleviate inflammation by attenuating phagocyte invasion in eccentrically contracted skeletal muscles.
Identifiants
pubmed: 38635146
doi: 10.1007/s10974-024-09672-w
pii: 10.1007/s10974-024-09672-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : the Japan Society for the Promotion of Science, Grants-in-Aid for Scientific Research
ID : 18K17839
Organisme : the Japan Society for the Promotion of Science, Grants-in-Aid for Scientific Research
ID : 23K10714
Informations de copyright
© 2024. The Author(s).
Références
Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88:287–332
doi: 10.1152/physrev.00015.2007
pubmed: 18195089
Allen DG, Whitehead NP, Froehner SC (2016) Absence of dystrophin disrupts skeletal muscle signaling: roles of Ca
doi: 10.1152/physrev.00007.2015
pubmed: 26676145
Amanzada A, Malik IA, Blaschke M, Khan S, Rahman H, Ramadori G, Moriconi F (2013) Identification of CD68(+) neutrophil granulocytes in in vitro model of acute inflammation and inflammatory bowel disease. Int J Clin Exp Pathol 6:561–570
pubmed: 23573303
pmcid: 3606846
Andrew PJ, Mayer B (1999) Enzymatic function of nitric oxide synthases. Cardiovasc Res 43:521–531
doi: 10.1016/S0008-6363(99)00115-7
pubmed: 10690324
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
doi: 10.1016/0003-2697(76)90527-3
pubmed: 942051
Corona BT, Balog EM, Doyle JA, Rupp JC, Luke RC, Ingalls CP (2010) Junctophilin damage contributes to early strength deficits and EC coupling failure after eccentric contractions. Am J Physiol 298:C365–C376
doi: 10.1152/ajpcell.00365.2009
Damoiseaux JG, Döpp EA, Calame W, Chao D, MacPherson GG, Dijkstra CD (1994) Rat macrophage lysosomal membrane antigen recognized by monoclonal antibody ED1. Immunology 83:140–147
pubmed: 7821959
pmcid: 1415006
Dutka TL, Mollica JP, Lamb GD (2011) Differential effects of peroxynitrite on contractile protein properties in fast- and slow-twitch skeletal muscle fibers of rat. J Appl Physiol 110:705–716
doi: 10.1152/japplphysiol.00739.2010
pubmed: 21030671
Gabriel A, Porrino ML, Stephenson LL, Zamboni WA (2004) Effect of L-arginine on leukocyte adhesion in ischemia-reperfusion injury. Plast Reconstr Surg 113:1698–1702
doi: 10.1097/01.PRS.0000117364.53547.0E
pubmed: 15114131
Ghimire K, Altmann HM, Straub AC, Isenberg JS (2017) Nitric oxide: what’s new to NO? Am J Physiol 312:C254–C262
doi: 10.1152/ajpcell.00315.2016
Hnia K, Gayraud J, Hugon G, Ramonatxo M, Porte SDL, Matecki S, Mornet D (2008) L-arginine decreases inflammation and modulates the nuclear factor-κB/matrix metalloproteinase cascade in mdx muscle fibers. Am J Pathol 172:1509–1519
doi: 10.2353/ajpath.2008.071009
pubmed: 18458097
pmcid: 2408412
Hody S, Croisier JL, Bury T, Rogister B, Leprince P (2019) Eccentric muscle contractions: risks and benefits. Front Physiol 10:536
doi: 10.3389/fphys.2019.00536
pubmed: 31130877
pmcid: 6510035
Kamandulis S, de Souza LF, Hernandez A, Katz A, Brazaitis M, Bruton JD, Venckunas T, Masiulis N, Mickeviciene D, Eimantas N, Subocius A, Rassier DE, Skurvydas A, Ivarsson N, Westerblad H (2017) Prolonged force depression after mechanically demanding contractions is largely independent of Ca
doi: 10.1096/fj.201700019R
pubmed: 28716970
Kanzaki K, Watanabe D, Aibara C, Kawakami Y, Yamada T, Takahashi Y, Wada M (2018) L-arginine ingestion inhibits eccentric contraction-induced proteolysis and force deficit via S-nitrosylation of calpain. Physiol Rep 6:e13582
doi: 10.14814/phy2.13582
pubmed: 29368397
pmcid: 5789731
Kanzaki K, Watanabe D, Aibara C, Kawakami Y, Yamada T, Takahashi Y, Wada M (2019) Ingestion of soy protein isolate attenuates eccentric contraction-induced force depression and muscle proteolysis via inhibition of calpain-1 activation in rat fast-twitch skeletal muscle. Nutrition 58:23–29
doi: 10.1016/j.nut.2018.06.025
pubmed: 30273822
Kanzaki K, Watanabe D, Kuratani M, Yamada T, Matsunaga S, Wada M (2017) Role of calpain in eccentric contraction-induced proteolysis of Ca
doi: 10.1152/japplphysiol.00270.2016
pubmed: 27979982
Kanzaki K, Watanabe D, Shi J, Wada M (2022) Mechanisms of eccentric contraction-induced muscle damage and nutritional supplementations for mitigating it. J Muscle Res Cell Motil 43:147–156
doi: 10.1007/s10974-022-09625-1
pubmed: 35854160
Klatt P, Schmidt K, Lehner D, Glatter O, Bachinger HP, Mayer B (1995) Structural-analysis of porcine brain nitric-oxide synthase reveals a role for tetrahydrobiopterin and L-arginine in the formation of an sds-resistant dimer. Embo J 14:3687–3695
doi: 10.1002/j.1460-2075.1995.tb00038.x
pubmed: 7543842
pmcid: 394443
Lapointe BM, Frenette J, Cote CH (2002) Lengthening contraction-induced inflammation is linked to secondary damage but devoid of neutrophil invasion. J Appl Physiol (1985) 92:1995–2004
doi: 10.1152/japplphysiol.00803.2001
pubmed: 11960950
Lomonosova YN, Shenkman BS, Kalamkarov GR, Kostrominova TY, Nemirovskaya TL (2014) L-arginine supplementation protects exercise performance and structural integrity of muscle fibers after a single bout of eccentric exercise in rats. PLoS ONE 9:e94448
doi: 10.1371/journal.pone.0094448
pubmed: 24736629
pmcid: 3988069
MacNeil LG, Baker SK, Stevic I, Tarnopolsky MA (2011) 17beta-estradiol attenuates exercise-induced neutrophil infiltration in men. Am J Physiol 300:R1443–R1451
Pandya CD, Lee B, Toque HA, Mendhe B, Bragg RT, Pandya B, Atawia RT, Isales C, Hamrick M, Caldwell RW, Fulzele S (2019) Age-dependent oxidative stress elevates arginase 1 and uncoupled nitric oxide synthesis in skeletal muscle of aged mice. Oxid Med Cell Longev 2019:1704650
doi: 10.1155/2019/1704650
pubmed: 31205583
pmcid: 6530149
Paulsen G, Crameri R, Benestad HB, Fjeld JG, Morkrid L, Hallen J, Raastad T (2010) Time course of leukocyte accumulation in human muscle after eccentric exercise. Med Sci Sports Exerc 42:75–85
doi: 10.1249/MSS.0b013e3181ac7adb
pubmed: 20010127
Peake JM, Neubauer O, Della Gatta PA, Nosaka K (2017) Muscle damage and inflammation during recovery from exercise. J Appl Physiol (1985) 122:559–570
doi: 10.1152/japplphysiol.00971.2016
pubmed: 28035017
Pizza FX, Peterson JM, Baas JH, Koh TJ (2005) Neutrophils contribute to muscle injury and impair its resolution after lengthening contractions in mice. J Physiol 562:899–913
doi: 10.1113/jphysiol.2004.073965
pubmed: 15550464
Sakurai T, Kashimura O, Kano Y, Ohno H, Ji LL, Izawa T, Best TM (2013) Role of nitric oxide in muscle regeneration following eccentric muscle contractions in rat skeletal muscle. J Physiol Sci 63:263–270
doi: 10.1007/s12576-013-0262-y
pubmed: 23606218
pmcid: 10717722
Shafat A, Butler P, Jensen RL, Donnelly AE (2004) Effects of dietary supplementation with vitamins C and E on muscle function during and after eccentric contractions in humans. Eur J Appl Physiol 93:196–202
doi: 10.1007/s00421-004-1198-y
pubmed: 15309547
Sloboda DD, Brown LA, Brooks SV (2018) Myeloid cell responses to contraction-induced injury differ in muscles of young and old mice. J Gerontol A Biol Sci Med Sci 73:1581–1590
doi: 10.1093/gerona/gly086
pubmed: 29684112
pmcid: 6230214
Voisin V, Sebrie C, Matecki S, Yu H, Gillet B, Ramonatxo M, Israel M, De la Porte S (2005) L-arginine improves dystrophic phenotype in mdx mice. Neurobiol Dis 20:123–130
doi: 10.1016/j.nbd.2005.02.010
pubmed: 16137573
Whiteman M, Armstrong JS, Cheung NS, Siau JL, Rose P, Schantz JT, Jones DP, Halliwell B (2004) Peroxynitrite mediates calcium-dependent mitochondrial dysfunction and cell death via activation of calpains. FASEB J 18:1395–1397
doi: 10.1096/fj.03-1096fje
pubmed: 15240564
Zhang BT, Whitehead NP, Gervasio OL, Reardon TF, Vale M, Fatkin D, Dietrich A, Yeung EW, Allen DG (2012) Pathways of Ca
doi: 10.1152/japplphysiol.00770.2011
pubmed: 22461447
pmcid: 3378392
Zou MH, Shi C, Cohen RA (2002) Oxidation of the zinc-thiolate complex and uncoupling of endothelial nitric oxide synthase by peroxynitrite. J Clin Invest 109:817–826
doi: 10.1172/JCI0214442
pubmed: 11901190
pmcid: 150913