Home LiteratureArticle Details
PMID: 15616319 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Hemolysis of erythrocytes by granulysin-derived peptides but not by granulysin.

Antimicrobial agents and chemotherapy ·Vol. 49 ·No. 1 ·2005-01-00 ·Pages 388-97

Li Q, Dong C, Deng A, Katsumata M, Nakadai A, Kawada T, Okada S, Clayberger C, Krensky AM

Abstract

Granulysin, a 9-kDa protein localized in human cytolytic T lymphocytes and natural killer cell granules, is cytolytic against tumors and microbes but not against red blood cells. Synthetic peptides corresponding to the central region of granulysin recapitulate the lytic activity of the intact molecule, and some peptides cause hemolysis of red blood cells. Peptides in which cysteine residues were replaced by serine maintain their activity against microbes but lose activity against human cells, suggesting their potential as antibiotics. Studies were undertaken to determine the mechanism of resistance of red blood cells to granulysin and sensitivity to a subset of granulysin-derived peptides. Granulysin lyses immature reticulocytes, which have mitochondria, but not red blood cells. Granulysin lyses U937 cells but not U937 cells lacking mitochondrial DNA and a functional respiratory chain (U937rho(o) degrees cells), further demonstrating the requirement of intact mitochondria for granulysin-mediated death. Peptide G8, which corresponds to helix 2/loop 2/helix 3, lyses red blood cells, while peptide G9, which is identical except that the cysteine residues were replaced by serine, does not lyse red blood cells. Granulysin peptide-induced hemolysis is markedly inhibited by an anion transporter inhibitor and by Na(+), K(+), and Ca(2+) channel blockers but not by Na(+)/K(+) pump, cotransport, or Cl(-) channel blockers. Although recombinant granulysin and G9 peptide do not induce hemolysis, they both competitively inhibit G8-induced hemolysis. The finding that some derivatives of granulysin are hemolytic may have important implications for the design of granulysin-based antimicrobial therapeutics.

MeSH Terms
Amino Acid Sequence Animals Antigens, Differentiation, T-Lymphocyte/chemistry,genetics,pharmacology Cells, Cultured Cytotoxicity, Immunologic Erythrocytes/drug effects Hemolysis/drug effects Humans Ion Channels/drug effects Killer Cells, Natural/immunology Molecular Sequence Data Peptides/chemical synthesis,chemistry,pharmacology Rabbits T-Lymphocytes, Cytotoxic/immunology
Chemicals
Antigens, Differentiation, T-Lymphocyte GNLY protein, human Ion Channels Peptides
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Li Qing
Division of Immunology and Transplantation Biology, Department of Pediatrics, Stanford University School of Medicine, 300 Pasteur Dr., Stanford, CA 94305, USA.
Dong Chen
Deng Anmei
Katsumata Masao
Nakadai Ari
Kawada Tomoyuki
Okada Satoshi
Clayberger Carol
Krensky Alan M
References (42)
42 references, click to expand
  1. Bactericidal and tumoricidal activities of synthetic peptides derived from granulysin.
    J Immunol. 2000 Aug 1;165(3):1486-90 PMID: 10903754
  2. The function of calcium in the potassium permeability of human erythrocytes.
    Biochim Biophys Acta. 1958 Dec;30(3):653-4 PMID: 13618284
  3. Granulysin, a T cell product, kills bacteria by altering membrane permeability.
    J Immunol. 2000 Dec 15;165(12):7102-8 PMID: 11120840
  4. K-Cl cotransport: properties and molecular mechanism.
    Cell Physiol Biochem. 2000;10(5-6):341-54 PMID: 11125215
  5. Ionic basis for membrane potential changes induced by hypoosmotic stress in guinea-pig ventricular myocytes.
    Cardiovasc Res. 2001 Jul;51(1):59-70 PMID: 11399248
  6. A distinct pathway of cell-mediated apoptosis initiated by granulysin.
    J Immunol. 2001 Jul 1;167(1):350-6 PMID: 11418670
  7. Multiple transport functions of a red blood cell anion exchanger, tAE1: its role in cell volume regulation.
    J Physiol. 2001 Sep 1;535(Pt 2):497-506 PMID: 11533139
  8. Activation of connexin-43 hemichannels can elevate [Ca(2+)]i and [Na(+)]i in rabbit ventricular myocytes during metabolic inhibition.
    J Mol Cell Cardiol. 2001 Dec;33(12):2145-55 PMID: 11735261
  9. Swelling-induced K(+) fluxes in vascular smooth muscle cells are mediated by charybdotoxin-sensitive K(+) channels.
    Cell Physiol Biochem. 2001;11(6):295-310 PMID: 11832655
  10. Oxidation induces a Cl(-)-dependent cation conductance in human red blood cells.
    J Physiol. 2002 Mar 15;539(Pt 3):847-55 PMID: 11897854
  11. Chlorodinitrobenzene-mediated damage in the human erythrocyte membrane leads to haemolysis.
    Life Sci. 2002 Jul 5;71(7):735-46 PMID: 12074932
  12. Glycophorin A-mediated haemolysis of normal human erythrocytes: evidence for antigen aggregation in the pathogenesis of immune haemolysis.
    Br J Haematol. 2002 Sep;118(3):899-908 PMID: 12181064
  13. ATP-sensitive K+ and Ca2+-activated K+ channels in lamprey ( Petromyzon marinus) red blood cell membrane.
    Pflugers Arch. 2002 Oct;445(1):152-60 PMID: 12397400
  14. Purification, characterization and molecular cloning of Vibrio fluvialis hemolysin.
    Biochim Biophys Acta. 2002 Sep 23;1599(1-2):106-14 PMID: 12479411
  15. Granulysin crystal structure and a structure-derived lytic mechanism.
    J Mol Biol. 2003 Jan 10;325(2):355-65 PMID: 12488100
  16. An improved method for detecting red cells with hemoglobin H inclusions that does not require glass capillary tubes.
    Clin Lab Haematol. 2003 Apr;25(2):87-91 PMID: 12641611
  17. Intracellular mediators of granulysin-induced cell death.
    J Immunol. 2003 Sep 1;171(5):2556-62 PMID: 12928406
  18. Role of Ca2+-activated K+ channels in human erythrocyte apoptosis.
    Am J Physiol Cell Physiol. 2003 Dec;285(6):C1553-60 PMID: 14600080
  19. The antiviral activity of the CXCR4 antagonist AMD3100 is independent of the cytokine-induced CXCR4/HIV coreceptor expression level.
    AIDS Res Hum Retroviruses. 2003 Dec;19(12):1135-9 PMID: 14709250
  20. Initiation of haemoglobin synthesis by methionyl-tRNA.
    Nature. 1970 Aug 29;227(5261):913-8 PMID: 4915406
  21. Mechanism of hemolysis induced by ferriprotoporphyrin IX.
    J Clin Invest. 1981 Sep;68(3):672-7 PMID: 7276166
  22. Properties of the Na+-K+ pump in human red cells with increased number of pump sites.
    J Clin Invest. 1987 Jul;80(1):128-37 PMID: 2439543
  23. Action mechanism of amphipathic peptides gramicidin S and melittin on erythrocyte membrane.
    Biochim Biophys Acta. 1988 Mar 22;939(1):57-63 PMID: 2450585
  24. High affinity inhibition of Ca(2+)-dependent K+ channels by cytochrome P-450 inhibitors.
    J Biol Chem. 1992 Jun 15;267(17):11789-93 PMID: 1376313
  25. Erythrocyte K-Cl cotransport: properties and regulation.
    Am J Physiol. 1992 Nov;263(5 Pt 1):C917-32 PMID: 1443104
  26. Imidazole antimycotics inhibitors of cytochrome P450 increase phosphatidylserine synthesis similarly to K(+)-channel blockers in Jurkat T cells.
    FEBS Lett. 1993 Mar 15;319(1-2):155-8 PMID: 8454049
  27. Characteristics of hyaluronidase and hemolytic activity in fishing tentacle nematocyst venom of Chrysaora quinquecirrha.
    Toxicon. 1994 Feb;32(2):165-74 PMID: 7908765
  28. Physiological roles and properties of potassium channels in arterial smooth muscle.
    Am J Physiol. 1995 Apr;268(4 Pt 1):C799-822 PMID: 7733230
  29. Apoptosis-associated derangement of mitochondrial function in cells lacking mitochondrial DNA.
    Cancer Res. 1996 May 1;56(9):2033-8 PMID: 8616847
  30. Effects of hyperthermia on intracellular chloride.
    J Membr Biol. 1996 Aug;152(3):217-22 PMID: 8672083
  31. Effects of gramicidin and tryptophan-N-formylated gramicidin on the sodium and potassium content of human erythrocytes.
    Mol Membr Biol. 1996 Oct-Dec;13(4):225-32 PMID: 9116761
  32. Processing, subcellular localization, and function of 519 (granulysin), a human late T cell activation molecule with homology to small, lytic, granule proteins.
    J Immunol. 1997 Mar 15;158(6):2680-8 PMID: 9058801
  33. Erythrocyte membrane transport physiology.
    Curr Opin Hematol. 1997 Mar;4(2):122-7 PMID: 9107529
  34. Granulysin, a new human cytolytic granule-associated protein with possible involvement in cell-mediated cytotoxicity.
    Semin Immunol. 1997 Apr;9(2):117-25 PMID: 9194222
  35. Two distinct K+ channels in lamprey (Lampetra fluviatilis) erythrocyte membrane characterized by single channel patch clamp.
    J Membr Biol. 1998 May 1;163(1):47-53 PMID: 9569249
  36. Distinct mechanisms for K+ efflux, intoxication, and hemolysis by Bordetella pertussis AC toxin.
    J Biol Chem. 1998 Jul 17;273(29):18260-7 PMID: 9660789
  37. Chloride and non-selective cation channels in unstimulated trout red blood cells.
    J Physiol. 1998 Aug 15;511 ( Pt 1):213-24 PMID: 9679175
  38. An antimicrobial activity of cytolytic T cells mediated by granulysin.
    Science. 1998 Oct 2;282(5386):121-5 PMID: 9756476
  39. The action of blocking agents applied to the inner face of Ca(2+)-activated K+ channels from human erythrocytes.
    J Membr Biol. 1998 Sep 15;165(2):133-43 PMID: 9745001
  40. Characterization of a haemolytic factor from Candida albicans.
    Microbiology. 1999 Mar;145 ( Pt 3):689-94 PMID: 10217503
  41. Biosynthesis of granulysin, a novel cytolytic molecule.
    Mol Immunol. 1999 May;36(7):413-22 PMID: 10449094
  42. Haemolysis of human and sheep red blood cells in glycerol media: the effect of pH and the role of band 3.
    Comp Biochem Physiol A Mol Integr Physiol. 2000 Nov;127(3):347-53 PMID: 11118944
Article Info
Journal
Antimicrobial agents and chemotherapy
Abbr.
Antimicrob Agents Chemother
ISSN
0066-4804
Published
2005-01-00
Pages
388-97
Language
English
Region
United States
NLM ID
0315061
PMCID
PMC538851
Subset
IM
Grants
NIAID NIH HHS · R01 AI043348 · United States
NIAID NIH HHS · R01 AI43348 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com