CoChat
Sign Up
Cited by 122Ion channel regulation and functionMuscle Physiology and DisordersImmune cells in cancer

Interactions between neutrophils and macrophages promote macrophage killing of rat muscle cells in vitro

Open access
Nguyen, H. X, Tidball, J. G·2003·The Journal of Physiology
DOI 10.1113/jphysiol.2002.031450PMC PMC2342622
Open this paper in CoChat — free account

Abstract

Current evidence indicates that the physiological functions of inflammatory cells are highly sensitive to their microenvironment, which is partially determined by the inflammatory cells and their potential targets. In the present investigation, interactions between neutrophils, macrophages and muscle cells that may influence muscle cell death are examined. Findings show that in the absence of macrophages, neutrophils kill muscle cells in vitro by superoxide-dependent mechanisms, and that low concentrations of nitric oxide (NO) protect against neutrophil-mediated killing. In the absence of neutrophils, macrophages kill muscle cells through a NO-dependent mechanism, and the presence of target muscle cells causes a three-fold increase in NO production by macrophages, with no change in the concentration of inducible nitric oxide synthase. Muscle cells that are co-cultured with both neutrophils and macrophages in proportions that are observed in injured muscle show cytotoxicity through a NO-dependent, superoxide-independent mechanism. Furthermore, the concentration of myeloid cells that is necessary for muscle killing is greatly reduced in assays that use mixed myeloid cell populations, rather than uniform populations of neutrophils or macrophages. These findings collectively show that the magnitude and mechanism of muscle cell killing by myeloid cells are modified by interactions between muscle cells and neutrophils, between muscle cells and macrophages and between macrophages and neutrophils.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1113/jphysiol.2002.031450

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Proinflammatory cytokines may inhibit muscle progenitor cell differentiation, and reactive oxygen species (nitric oxide) from M1 cells can be cytotoxic in sufficient quantities, requiring resolution of the proinflammatory response for muscle recovery.

    “However, it has also been shown that proinflammatory cytokines may inhibit muscle progenitor cell differentiation and that the reactive oxygen species that are produced by M1 cells (nitric oxide) can be cytotoxic if present in sufficient quantities, demonstrating the need for resolution of the proinflammatory response for muscle recovery to proceed beyond this initial stage [120–122].”

    From Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine (2012) · cites this paper as [120]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

No citation lists for this paper

No citation lists for this paper yet — checked again daily.

References 33 · Cited by 122

Research works printed but not linked: 32

  1. Abu-Soud HM, Hazen SL. Nitric oxide modulates the catalytic activity of myeloperoxidase. J Biol Chem. 2000;275:5425–5430. doi: 10.1074/jbc.275.8.5425. [DOI] [PubMed] [Google Scholar] · DOI
  2. Amano F, Noda T. Improved detection of nitric oxide radical (NO) production in an activated macrophage culture with a radical scavenger, carboxy PTIO, and Griess reagent. FEBS Letters. 1995;368:425–428. doi: 10.1016/0014-5793(95)00700-j. [DOI] [PubMed] [Google Scholar] · DOI
  3. Blaylock MG, Cuthbertson BH, Galley HF, Ferguson N, Webster NR. The effect of nitric oxide and peroxynitrite on apoptosis in human polymorphonuclear leukocytes. Free Rad Biol Med. 1998;25:748–752. doi: 10.1016/s0891-5849(98)00108-7. [DOI] [PubMed] [Google Scholar] · DOI
  4. Dijkstra CD, Dopp EA, Joling P, Kraal G. The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunol. 1985;54:589–599. [PMC free article] [PubMed] [Google Scholar]
  5. Fortenberry JD, Owens ML, Brown LA. S-nitrosoglutathione enhances neutrophil DNA fragmentation and cell death. Am J Physiol. 1990;276:L435–442. doi: 10.1152/ajplung.1999.276.3.L435. [DOI] [PubMed] [Google Scholar] · DOI
  6. Gryglewski RJ, Palmer RM, Moncada S. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature. 1986;320:454–456. doi: 10.1038/320454a0. [DOI] [PubMed] [Google Scholar] · DOI
  7. Gupta MP, Evanoff V, Hart CM. Nitric oxide attenuates hydrogen peroxide-mediated injury to porcine pulmonary artery endothelial cells. Am J Physiol. 1997;272:L1133–1141. doi: 10.1152/ajplung.1997.272.6.L1133. [DOI] [PubMed] [Google Scholar] · DOI
  8. Hohlfeld R, Engel AG. Lysis of myotubes by alloreactive cytotoxic T cells and natural killer cells. Relevance to myoblast transplantation. J Clin Invest. 1990;86:370–374. doi: 10.1172/JCI114711. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  9. Hopkinson-Woolley J, Hughes D, Gordon S, Martin P. Macrophage recruitment during limb development and wound healing in the embryonic and foetal mouse. J Cell Sci. 1994;107:1159–1167. doi: 10.1242/jcs.107.5.1159. [DOI] [PubMed] [Google Scholar] · DOI
  10. Koh TJ, Tidball JG. Nitric oxide inhibits calpain-mediated proteolysis of talin in skeletal muscle cells. Am J Physiol Cell Physiol. 2000;279:C806–812. doi: 10.1152/ajpcell.2000.279.3.C806. [DOI] [PubMed] [Google Scholar] · DOI
  11. Markey BA, Phan SH, Varani J, RyaN US, Ward PA. Inhibition of cytotoxicity by intracellular superoxide dismutase supplementation. Free Rad Biol Med. 1990;9:307–314. doi: 10.1016/0891-5849(90)90005-4. [DOI] [PubMed] [Google Scholar] · DOI
  12. Massimino ML, Rapizzi E, Cantini M, Dalla LiberaL, Mazzoleni F, Arslan P, Carraro U. ED2+ macrophages increase selectively myoblast proliferation in muscle cultures. Biochem Biophys Res Commun. 1997;235:754–759. doi: 10.1006/bbrc.1997.6823. [DOI] [PubMed] [Google Scholar] · DOI
  13. Meszaros AJ, Reichner JS, Albina JE. Macrophage-induced neutrophil apoptosis. J Immunol. 2000;165:435–441. doi: 10.4049/jimmunol.165.1.435. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  14. Miles AM, Bohle DS, Glassbrenner PA, Hansert B, Wink DA, Grisham MB. Modulation of superoxide-dependent oxidation and hydroxylation reactions by nitric oxide. J Biol Chem. 1996;271:40–47. doi: 10.1074/jbc.271.1.40. [DOI] [PubMed] [Google Scholar] · DOI
  15. Moilanen E, Vapaatalo H. Nitric oxide in inflammation and immune response. Ann Med. 1995;27:359–367. doi: 10.3109/07853899509002589. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  16. Palmer RM, Bridge L, Foxwell NA, Moncada S. The role of nitric oxide in endothelial cell damage and its inhibition by glucocorticoids. Br J Pharmacol. 1992;105:11–12. doi: 10.1111/j.1476-5381.1992.tb14202.x. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  17. Pan J, Burgher KL, Szczepanik AM, Ringheim GE. Tyrosine phosphorylation of inducible nitric oxide synthase: implications for potential post-translational regulation. Biochem J. 1996;314:889–894. doi: 10.1042/bj3140889. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  18. Radomski MW, Palmer RM, Moncada S. Glucocorticoids inhibit the expression of an inducible, but not the constituitive, nitric oxide synthase in vascular endothelial cells. Proc Natl Acad Sci U S A. 1990;87:10043–10047. doi: 10.1073/pnas.87.24.10043. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  19. Rando TA, Disatnik MH, Franco A. Muscle cells from mdx mice have an increased susceptibility to oxidative stress. Neuromuscul Disorders. 1998;8:14–21. doi: 10.1016/s0960-8966(97)00124-7. [DOI] [PubMed] [Google Scholar] · DOI
  20. Robertson TA, Maley MaL, Grounds MD, Papadimitriou J. The role of macrophages in skeletal muscle regeneration with particular reference to chemotaxis. Exp Cell Res. 1993;207:321–331. doi: 10.1006/excr.1993.1199. [DOI] [PubMed] [Google Scholar] · DOI
  21. Simchowitz L, Spilberg I. Evidence for the role of superoxide radicals in neutrophil-mediated cytotoxicity. Immunol. 1979;37:301–309. [PMC free article] [PubMed] [Google Scholar]
  22. Srinivasan R, Buchweitz J, Ganey PE. Alteration by fluramide of neutrophil response to stimulation. Biochem Pharmacol. 1997;53:1179–1185. doi: 10.1016/s0006-2952(97)00099-3. [DOI] [PubMed] [Google Scholar] · DOI
  23. Stamler JS, Meissner G. Physiology of nitric oxide in skeletal muscle. Physiol Rev. 2001;81:209–237. doi: 10.1152/physrev.2001.81.1.209. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  24. St Pierre BA, Tidball JG. Differential response of macrophage subpopulations to soleus muscle reloading after hindlimb suspension. J Appl Physiol. 1994;77:290–297. doi: 10.1152/jappl.1994.77.1.290. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  25. Talpain E, Armstrong RA, Coleman RA, Vardey CJ. Characterization of the PGE receptor subtype mediating inhibition of superoxide production in human neutrophils. Br J Pharmacol. 1995;114:1459–1465. doi: 10.1111/j.1476-5381.1995.tb13370.x. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  26. Tidball JG, Berchenko E, Frenette J. Macrophage invasion does not contribute to muscle membrane injury during inflammation. J Leukoc Biol. 1999;65:492–498. [PubMed] [Google Scholar]
  27. Tidball JG, Lavergne E, Lau KS, Spencer MJ, Stull JT, Wehling M. Mechanical loading regulates nitric oxide synthase expression and activity in developing and adult skeletal muscle. Am J Physiol. 1998;275:C260–266. doi: 10.1152/ajpcell.1998.275.1.C260. [DOI] [PubMed] [Google Scholar] · DOI
  28. Ward C, Wong TH, Murray J, Rahman I, Haslett C, Chilvers ER, Rossi AG. Induction of human neutrophil apoptosis by nitric oxide donors: evidence for a caspase-dependent, cyclic-GMP-independent, mechanism. Biochem Pharmacol. 2000;59:305–314. doi: 10.1016/s0006-2952(99)00329-9. [DOI] [PubMed] [Google Scholar] · DOI
  29. Wehling M, Spencer MJ, Tidball JG. A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J Cell Biol. 2001;155:123–131. doi: 10.1083/jcb.200105110. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  30. Wink DA, Hanbauer J, Krishna MC, Degraff W, Gamson J, Mitchell JB. Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc Natl Acad Sci U S A. 1993;90:9813–9817. doi: 10.1073/pnas.90.21.9813. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  31. Wink DA, Hanbauer I, GrishaM MB, Laval F, Nims RW, Laval J, Cook J, Pacelli R, Liebmann J, Krishna M, Ford PC, Mitchell JB. Chemical biology of nitric oxide: regulation and protective and toxic mechanisms. Curr Top Cell Regul. 1996;34:159–187. doi: 10.1016/s0070-2137(96)80006-9. [DOI] [PubMed] [Google Scholar] · DOI
  32. Zhuang W, Eby JC, Cheong M, Mohaatra PK, BredT DS, Disatnik M, Rando TA. The susceptibility of muscle cells to oxidative stress is independent of nitric oxide synthase expression. Muscle Nerve. 2001;24:502–511. doi: 10.1002/mus.1033. [DOI] [PubMed] [Google Scholar] · DOI

Authors
Nguyen, H. X., & Tidball, J. G.
Affiliations
University of California, Los Angeles (US)
ORCID
Venue
The Journal of Physiology
Publisher
Wiley
Published
2002-12-20
Volume
547
Issue
1
Pages
125-132
ISSN
0022-3751 (ISSN-L)
DOI
10.1113/jphysiol.2002.031450
PMC
PMC2342622
OpenAlex
W4251296644
Cited by
122
References
33
Citations by year
2026: 2 · 2025: 4 · 2024: 3 · 2023: 2 · 2022: 5 · 2021: 4 · 2020: 10 · 2019: 5 · 2018: 6 · 2017: 2 · 2016: 6 · 2015: 5 · 2014: 3 · 2013: 10 · 2012: 12
FWCI
0.58
Type
journal article
Language
en
Open access
Licence
doi.wiley.com/10.1002/tdm_license_1 (tdm, 4638 d)
Locations
  • The Journal of Physiology (publishedVersion)
  • PubMed Central (publishedVersion)
Funders
  • National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR047855, AR47855-01, AR-40343, AR/HD47721)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD047721)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
  • Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Keywords
neutrophils, macrophages, neutrophil-macrophage interaction, macrophage killing, muscle cells, HCN channels, hyperpolarization-activated cation channels, peristaltic contractions, upper urinary tract, evolutionary conservation

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review