Altered exosomal protein expression in the serum of NF-κB knockout mice following skeletal muscle ischemia-reperfusion injury

Journal of Biomedical Science

Volumn 22, Issue 1, 2015, Pages

  Yang, Johnson Chia Shen ^a   Lin, Ming Wei ^a   Rau, Cheng Shyuan ^a   Jeng, Seng Feng ^b   Lu, Tsu Hsiang ^a   Wu, Yi Chan ^a   Chen, Yi Chun ^a   Tzeng, Siou Ling ^a   Wu, Chia Jung ^a   Hsieh, Ching Hua ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b I SHOU UNIVERSITY   (Taiwan)

Author keywords

Exosome; Muscle ischemia reperfusion (I R) injury; NF B; Proteomics; Two dimensional gel electrophoresis

Indexed keywords

ADENYLOSUCCINATE SYNTHASE; AMYLASE; APOLIPOPROTEIN B; COMPLEMENT COMPONENT C3; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN KAPPA CHAIN; PREGNANCY ASSOCIATED ALPHA2 GLYCOPROTEIN; PROTEOME; SYNAPTOTAGMIN I;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; C57BL 6 MOUSE; CONTROLLED STUDY; DOWN REGULATION; EXOSOME; HUMAN; HUMAN CELL; IMMUNOGLOBULIN BLOOD LEVEL; KNOCKOUT MOUSE; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; MOUSE; MUSCLE ISCHEMIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; REPERFUSION INJURY; SKELETAL MUSCLE; STIMULUS RESPONSE; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; UPREGULATION; ANIMAL; C57BL MOUSE; DEFICIENCY; GENETICS; METABOLISM; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; EXOSOMES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SKELETAL; NF-KAPPA B; PROTEOME; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

EID: 84931026064     PISSN: 10217770     EISSN: 14230127     Source Type: Journal    
DOI: 10.1186/s12929-015-0147-x     Document Type: Article

References (48)

1. Blaisdell FW. The pathophysiology of skeletal muscle ischemia and the reperfusion syndrome: a review. Cardiovasc Surg. 2002;10(6):620-30.
2. Walker PM. Ischemia/reperfusion injury in skeletal muscle. Ann Vasc Surg. 1991;5(4):399-402.
3. Lentsch AB, Yoshidome H, Warner RL, Ward PA, Edwards MJ. Secretory leukocyte protease inhibitor in mice regulates local and remote organ inflammatory injury induced by hepatic ischemia/reperfusion. Gastroenterology. 1999;117(4):953-61.
4. Lille ST, Lefler SR, Mowlavi A, Suchy H, Boyle Jr EM, Farr AL, et al. Inhibition of the initial wave of NF-kappaB activity in rat muscle reduces ischemia/reperfusion injury. Muscle Nerve. 2001;24(4):534-41.
5. Park JW, Qi WN, Cai Y, Urbaniak JR, Chen LE. Proteasome inhibitor attenuates skeletal muscle reperfusion injury by blocking the pathway of nuclear factor-kappaB activation. Plast Reconstr Surg. 2007;120(7):1808-18.
6. Kim YS1, Kim JS, Kwon JS, Jeong MH, Cho JG, Park JC, Kang JC, Ahn Y: BAY 11-7082, a nuclear factor-κB inhibitor, reduces inflammation and apoptosis in a rat cardiac ischemia-reperfusion injury model. International heart journal 2010;5(5):348-353.
7. Andrade-Silva AR, Ramalho FS, Ramalho LN, Saavedra-Lopes M, Jordao Jr AA, Vanucchi H, et al. Effect of NFkappaB inhibition by CAPE on skeletal muscle ischemia-reperfusion injury. J Surg Res. 2009;153(2):254-62.
8. Suzuki T, Yamashita K, Jomen W, Ueki S, Aoyagi T, Fukai M, et al. The novel NF-kappaB inhibitor, dehydroxymethylepoxyquinomicin, prevents local and remote organ injury following intestinal ischemia/reperfusion in rats. J Surg Res. 2008;149(1):69-75.
9. Burke M, Choksawangkarn W, Edwards N, Ostrand-Rosenberg S, Fenselau C. Exosomes from myeloid-derived suppressor cells carry biologically active proteins. J Proteome Res. 2014;13(2):836-43.
10. Yoon YJ, Kim OY, Gho YS. Extracellular vesicles as emerging intercellular communicasomes. BMB Reports 2014;47(10):531-539
11. Svensson KJ, Christianson HC, Wittrup A, Bourseau-Guilmain E, Lindqvist E, Svensson LM, et al. Exosome uptake depends on ERK1/2-heat shock protein 27 signaling and lipid Raft-mediated endocytosis negatively regulated by caveolin-1. J Biol Chem. 2013;288(24):17713-24.
12. Nanbo A, Kawanishi E, Yoshida R, Yoshiyama H. Exosomes derived from Epstein-Barr virus-infected cells are internalized via caveola-dependent endocytosis and promote phenotypic modulation in target cells. J Virol. 2013;87(18):10334-47.
13. Hudson MB, Woodworth-Hobbs ME, Zheng B, Rahnert JA, Blount MA, Gooch JL, et al. miR-23a is decreased during muscle atrophy by a mechanism that includes calcineurin signaling and exosome-mediated export. Am J Physiol Cell Physiol. 2014;306(6):C551-8.
14. Forterre A, Jalabert A, Chikh K, Pesenti S, Euthine V, Granjon A, et al. Myotube-derived exosomal miRNAs downregulate Sirtuin1 in myoblasts during muscle cell differentiation. Cell Cycle. 2014;13(1):78-89.
15. Ung TH, Madsen HJ, Hellwinkel JE, Lencioni AM, Graner MW. Exosome proteomics reveals transcriptional regulator proteins with potential to mediate downstream pathways. Cancer Sci. 2014;105(11):1384-1392
16. Jaworski E, Narayanan A, Van Duyne R, Shabbeer-Meyering S, Iordanskiy S, Saifuddin M, et al. Human T-lymphotropic Virus Type 1-infected Cells Secrete Exosomes That Contain Tax Protein. J Biol Chem. 2014;289(32):22284-305.
17. Beckham CJ, Olsen J, Yin PN, Wu CH, Ting HJ, Hagen FK, et al. Bladder cancer exosomes contain EDIL-3/Del1 and facilitate cancer progression. J Urol. 2014;192(2):583-92.
18. Fruhbeis C, Frohlich D, Kuo WP, Amphornrat J, Thilemann S, Saab AS, et al. Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyteneuron communication. PLoS Biol. 2013;11(7), e1001604.
19. Beninson LA, Fleshner M. Exosomes: An emerging factor in stress-induced immunomodulation. Seminars Immunol. 2014;26(5):394-401.
20. de Jong OG, Verhaar MC, Chen Y, Vader P, Gremmels H, Posthuma G, et al. Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes. J Extracellular Vesicles. 2012;1.
21. Robbins PD, Morelli AE. Regulation of immune responses by extracellular vesicles. Nat Rev Immunol. 2014;14(3):195-208.
22. Sonoda H, Yokota-Ikeda N, Oshikawa S, Kanno Y, Yoshinaga K, Uchida K, et al. Decreased abundance of urinary exosomal aquaporin-1 in renal ischemiareperfusion injury. Am J Physiol Renal Physiol. 2009;297(4):F1006-16.
23. Salomon C, Kobayashi M, Ashman K, Sobrevia L, Mitchell MD, Rice GE. Hypoxia-induced changes in the bioactivity of cytotrophoblast-derived exosomes. PLoS One. 2013;8(11), e79636.
24. Zhou H, Pisitkun T, Aponte A, Yuen PS, Hoffert JD, Yasuda H, et al. Exosomal Fetuin-A identified by proteomics: a novel urinary biomarker for detecting acute kidney injury. Kidney Int. 2006;70(10):1847-57.
25. Yang JC, Wu SC, Rau CS, Chen YC, Lu TH, Wu YC, et al. TLR4/NF-kappa B-Responsive MicroRNAs and Their Potential Target Genes: A Mouse Model of Skeletal Muscle Ischemia-Reperfusion. Injury. 2015;2015:410721.
26. Rau CS, Yang JC, Chen YC, Wu CJ, Lu TH, Tzeng SL, et al. Lipopolysaccharide-induced microRNA-146a targets CARD10 and regulates angiogenesis in human umbilical vein endothelial cells. Toxicol Sci. 2014;140(2):315-26.
27. Mi H, Muruganujan A, Casagrande JT, Thomas PD. Large-scale gene function analysis with the PANTHER classification system. Nat Protoc. 2013;8(8):1551-66.
28. Bellisola G, Casaril M, Gabrielli GB, Caraffi M, Corrocher R. Catalase activity in human hepatocellular carcinoma (HCC). Clin Biochem. 1987;20(6):415-7.
29. Dick RA, Kwak MK, Sutter TR, Kensler TW. Antioxidative function and substrate specificity of NAD(P)H-dependent alkenal/one oxidoreductase. A new role for leukotriene B4 12-hydroxydehydrogenase/15-oxoprostaglandin 13-reductase. J Biol Chem. 2001;276(44):40803-10.
30. Dinkova-Kostova AT, Talalay P. NAD(P)H:quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxidant enzyme and exceptionally versatile cytoprotector. Arch Biochem Biophys. 2010;501(1):116-23.
31. Brass EP, Hiatt WR, Gardner AW, Hoppel CL. Decreased NADH dehydrogenase and ubiquinol-cytochrome c oxidoreductase in peripheral arterial disease. Am J Physiol Heart Circ Physiol. 2001;280(2):H603-9.
32. del Zoppo GJ. In stroke, complement will get you nowhere. Nat Med. 1999;5(9):995-6.
33. Eisenhardt SU, Schmidt Y, Karaxha G, Iblher N, Penna V, Torio-Padron N, et al. Monitoring molecular changes induced by ischemia/reperfusion in human free muscle flap tissue samples. Ann Plast Surg. 2012;68(2):202-8.
34. Yang J, Ahn HN, Chang M, Narasimhan P, Chan PH, Song YS. Complement component 3 inhibition by an antioxidant is neuroprotective after cerebral ischemia and reperfusion in mice. J Neurochem. 2013;124(4):523-35.
35. Olsson S, Stokowska A, Holmegaard L, Jood K, Blomstrand C, Pekna M, et al. Genetic variation in complement component C3 shows association with ischaemic stroke. Eur J Neurol. 2011;18(10):1272-4.
36. Mocco J, Mack WJ, Ducruet AF, Sosunov SA, Sughrue ME, Hassid BG, et al. Complement component C3 mediates inflammatory injury following focal cerebral ischemia. Circ Res. 2006;99(2):209-17.
37. Moon MR, Parikh AA, Pritts TA, Fischer JE, Cottongim S, Szabo C, et al. Complement component C3 production in IL-1beta-stimulated human intestinal epithelial cells is blocked by NF-kappaB inhibitors and by transfection with ser 32/36 mutant IkappaBalpha. J Surg Res. 1999;82(1):48-55.
38. Skornicka EL, Kiyatkina N, Weber MC, Tykocinski ML, Koo PH. Pregnancy zone protein is a carrier and modulator of placental protein-14 in T-cell growth and cytokine production. Cell Immunol. 2004;232(1-2):144-56.
39. Chaitanya GV, Eeka P, Munker R, Alexander JS, Babu PP. Role of cytotoxic protease granzyme-b in neuronal degeneration during human stroke. Brain Pathol. 2011;21(1):16-30.
40. Sirover MA. Role of the glycolytic protein, glyceraldehyde-3-phosphate dehydrogenase, in normal cell function and in cell pathology. J Cell Biochem. 1997;66(2):133-40.
41. Yogalingam G, Hwang S, Ferreira JC, Mochly-Rosen D. Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) phosphorylation by protein kinase Cdelta (PKCdelta) inhibits mitochondria elimination by lysosomal-like structures following ischemia and reoxygenation-induced injury. J Biol Chemist. 2013;288(26):18947-60.
42. Tanaka R, Mochizuki H, Suzuki A, Katsube N, Ishitani R, Mizuno Y, et al. Induction of glyceraldehyde-3-phosphate dehydrogenase (GAPDH) expression in rat brain after focal ischemia/reperfusion. J Cereb Blood Flow Metab. 2002;22(3):280-8.
43. Hurt-Camejo E, Camejo G. Why are plasmatic apoB lipoproteins atherogenic? The hypothesis of response to retention. Investig Clin. 2001;42 Suppl 1:43-73.
44. Michiue T, Ishikawa T, Kawamoto O, Chen JH, Wang Q, Zhu BL, et al. Postmortem serum levels of amylase and gamma glutamyl transferase (GGT) as markers of systemic tissue damage in forensic autopsy. Legal Med. 2013;15(2):79-84.
45. Malinoski DJ, Hadjizacharia P, Salim A, Kim H, Dolich MO, Cinat M, et al. Elevated serum pancreatic enzyme levels after hemorrhagic shock predict organ failure and death. J Trauma. 2009;67(3):445-9.
46. Sokolowski A, Spormann H, Urbahn H, Letko G. Contribution of pancreatic edema and short-term ischemia to experimental acute pancreatitis in the rat. II. Behaviour of serum parameters. Zeitschrift fur experimentelle Chirurgie, Transplantation, und kunstliche Organe : Organ der Sektion Experimentelle Chirurgie der Gesellschaft fur Chirurgie der DDR. 1986;19(6):331-9.
47. Viola G, Al-Mufti RA, Sohail M, Williamson RC, Mathie RT. Nitric oxide induction in a rat model of selective pancreatic ischemia and reperfusion. Hepato-Gastroenterology. 2000;47(35):1250-5.
48. Parissis JT, Adamopoulos SN, Venetsanou KF, Karas SM, Kremastinos DT. Elevated plasma amylase levels in advanced chronic heart failure secondary to ischemic or idiopathic dilated cardiomyopathy: correlation with circulating interleukin-6 activity. J Interfero n Cytokine Res. 2003;23(6):329-33.