Proteomic Analysis of the Increased Proteins in Peroxiredoxin II Deficient RBCs

  • Yang, Hee-Young (Department of Oral Biochemistry, Dental Science Research Institute and the BK21 Project, Medical Research Center for Biomineralization Disorders, School of Dentistry, Chonnam National University) ;
  • Lee, Tae-Hoon (Department of Oral Biochemistry, Dental Science Research Institute and the BK21 Project, Medical Research Center for Biomineralization Disorders, School of Dentistry, Chonnam National University)
  • 투고 : 2012.03.19
  • 심사 : 2012.03.26
  • 발행 : 2012.03.31

초록

Peroxiredoxin II (Prdx II; a typical 2-Cys Prdx) has been originally isolated from erythrocytes, and its structure and peroxidase activity have been adequately studied. Prdx II has been reported to protect a wide range of cellular environments as antioxidant enzyme, and its dysfunctions may be implicated in a variety of disease states associated with oxidative stress, including cancer and aging-associated pathologies. But, the precise mechanism is still obscure in various aspects of aging containing ovarian aging. Identification and relative quantification of the increased proteins affected by Prdx II deficiency may help identify novel signaling mechanisms that are important for oxidative stress-related diseases. To identify the increased proteins in Prdx $II^{-/-}$ mice, we performed RBC comparative proteome analysis in membrane fraction and cytosolic fractions by nano-UPLC-$MS^E$ shotgun proteomics. We found the increased 86 proteins in membrane (32 proteins) and cytosolic (54 proteins) fractions, and analyzed comparative expression pattern in healthy RBCs of Prdx $II^{+/+}$ mice, healthy RBCs of Prdx $II^{-/-}$ mice, and abnormal RBCs of Prdx $II^{-/-}$ mice. These proteins belonged to cellular functions related with RBC lifespan maintain, such as cellular morphology and assembly, cell-cell interaction, metabolism, and stress-induced signaling. Moreover, protein networks among the increased proteins were analyzed to associate with various diseases. Taken together, RBC proteome may provide clues to understand the clue about redox-imbalanced diseases.

키워드

참고문헌

  1. Baker MA, Lawen A (2000): Plasma membrane NADH- oxidoreductase system: a critical review of the structural and functional data. Antioxidants & Redox Signaling 2:197-212. https://doi.org/10.1089/ars.2000.2.2-197
  2. Bosman GJ, Lasonder E, Groenen-Dopp YA, Willekens FL, Werre JM, Novotny VM (2010): Comparative proteomics of erythrocyte aging in vivo and in vitro. Journal of Proteomics 73:396-402. https://doi.org/10.1016/j.jprot.2009.07.010
  3. Broekmans FJ, Knauff EA, Te Velde ER, Macklon N S, Fauser BC (2007): Female reproductive ageing: current knowledge and future trends. Trends in Endocrinology and Metabolism: TEM 18:58-65. https://doi.org/10.1016/j.tem.2007.01.004
  4. Cha MK, Yun CH, Kim IH (2000): Interaction of human thiol-specific antioxidant protein 1 with erythrocyte plasma membrane. Biochemistry 39:6944-6950. https://doi.org/10.1021/bi000034j
  5. Chung Y, Park C, Kwon J, Kim S (2009): A fused silica micro-electrospray tip with an electrically floating metal wire insert to achieve more stable electrospray ionization. J Am Soc Mass Spectrom 20:751-754. https://doi.org/10.1016/j.jasms.2008.12.009
  6. De Franceschi L, Rivera A, Fleming MD, Honczarenko M, Peters LL, Gascard P, Mohandas N, Brugnara C (2005): Evidence for a protective role of the Gardos channel against hemolysis in murine spherocytosis. Blood 106:1454-1459. https://doi.org/10.1182/blood-2005-01-0368
  7. Hershko A, Ciechanover A (1998): The ubiquitin system. Annual Review of Biochemistry 67:425-479. https://doi.org/10.1146/annurev.biochem.67.1.425
  8. Iwahara S, Satoh H, Song DX, Webb J, Burlingame AL, Nagae Y, Muller-Eberhard U (1995): Purification, characterization, and cloning of a heme-binding protein (23 kDa) in rat liver cytosol. Biochemistry 34:13398-13406. https://doi.org/10.1021/bi00041a017
  9. Kakhniashvili DG, Bulla LA, Jr. & Goodman SR (2004): The human erythrocyte proteome: analysis by ion trap mass spectrometry. Molecular & Cellular Proteomics : MCP 3:501-509. https://doi.org/10.1074/mcp.M300132-MCP200
  10. Kakhniashvili DG, Griko NB, Bulla LA, Jr. & Goodman SR (2005): The proteomics of sickle cell disease: profiling of erythrocyte membrane proteins by 2D-DIGE and tandem mass spectrometry. Experimental Biology and Medicine 230:787-792. https://doi.org/10.1177/153537020523001102
  11. Khandros E, Weiss MJ (2010): Protein quality control during erythropoiesis and hemoglobin synthesis. Hematology/oncology Clinics of North America 24:1071-1088. https://doi.org/10.1016/j.hoc.2010.08.013
  12. Lee TH, Kim SU, Yu SL, Kim SH, Park DS, Moon HB, Dho SH, Kwon KS, Kwon HJ, Han YH, Jeong S, Kang SW, Shin HS, Lee KK, Rhee SG, Yu DY (2003): Peroxiredoxin II is essential for sustaining life span of erythrocytes in mice. Blood 101:5033-5038. https://doi.org/10.1182/blood-2002-08-2548
  13. Lim YS, Cha MK, Yun CH, Kim HK, Kim K, Kim IH (1994): Purification and characterization of thiol- specific antioxidant protein from human red blood cell: a new type of antioxidant protein. Biochem Biophys Res Commun 199:199-206. https://doi.org/10.1006/bbrc.1994.1214
  14. Low FM, Hampton MB, Peskin AV, Winterbourn CC (2007): Peroxiredoxin 2 functions as a noncatalytic scavenger of low-level hydrogen peroxide in the erythrocyte. Blood 109:2611-2617. https://doi.org/10.1182/blood-2006-09-048728
  15. Low FM, Hampton MB, Winterbourn CC (2008): Peroxiredoxin 2 and peroxide metabolism in the erythrocyte. Antioxid Redox Signal 10:1621-1630. https://doi.org/10.1089/ars.2008.2081
  16. Macfarlane AJ, Perry CA, Mcentee MF, Lin DM, Stover PJ (2011): Mthfd1 is a modifier of chemically induced intestinal carcinogenesis. Carcinogenesis 32: 427-433. https://doi.org/10.1093/carcin/bgq270
  17. Min-Oo G, Gros P (2005): Erythrocyte variants and the nature of their malaria protective effect. Cellular Microbiology 7:753-763. https://doi.org/10.1111/j.1462-5822.2005.00524.x
  18. Minetti M, Malorni W (2006): Redox control of red blood cell biology: the red blood cell as a target and source of prooxidant species. Antioxidants & Redox Signaling 8:1165-1169. https://doi.org/10.1089/ars.2006.8.1165
  19. Mostowska A, Myka M, Lianeri M, Roszak A, Jagodzinski PP (2011): Folate and choline metabolism gene variants and development of uterine cervical carcinoma. Clinical Biochemistry 44:596-600. https://doi.org/10.1016/j.clinbiochem.2011.02.007
  20. Nickel C, Rahlfs S, Deponte M, Koncarevic S, Becker K (2006): Thioredoxin networks in the malarial parasite Plasmodium falciparum. Antioxidants & Redox Signaling 8:1227-1239. https://doi.org/10.1089/ars.2006.8.1227
  21. Nohl H, Stolze K (1998): The effects of xenobiotics on erythrocytes. General Pharmacology 31:343-347. https://doi.org/10.1016/S0306-3623(97)00457-6
  22. Pasini EM, Kirkegaard M, Mortensen P, Lutz HU, Thomas AW, Mann M (2006): In-depth analysis of the membrane and cytosolic proteome of red blood cells. Blood 108:791-801. https://doi.org/10.1182/blood-2005-11-007799
  23. Pasini EM, Kirkegaard M, Salerno D, Mortensen P, Mann M, Thomas AW (2008): Deep coverage mouse red blood cell proteome: a first comparison with the human red blood cell. Molecular & Cellular Proteomics : MCP 7:1317-1330. https://doi.org/10.1074/mcp.M700458-MCP200
  24. Pasini EM, Lutz HU, Mann M, Thomas AW (2010): Red blood cell (RBC) membrane proteomics--Part II: Comparative proteomics and RBC patho-physiology. Journal of Proteomics 73:421-435. https://doi.org/10.1016/j.jprot.2009.07.004
  25. Peters LL, Shivdasani RA, Liu SC, Hanspal M, John KM, Gonzalez JM, Brugnara C, Gwynn B, Mohandas N, Alper SL, Orkin SH, Lux SE (1996): Anion exchanger 1 (band 3) is required to prevent erythrocyte membrane surface loss but not to form the membrane skeleton. Cell 86:917-927. https://doi.org/10.1016/S0092-8674(00)80167-1
  26. Rhee SG, Kang SW, Chang TS, Jeong W, Kim K (2001): Peroxiredoxin, a novel family of peroxidases. IUBMB Life 52:35-41. https://doi.org/10.1080/15216540252774748
  27. Roux-Dalvai F, Gonzalez De Peredo A, Simo C, Guerrier L, Bouyssie D, Zanella A, Citterio A, Burlet-Schiltz O, Boschetti E, Righetti PG, Monsarrat B (2008): Extensive analysis of the cytoplasmic proteome of human erythrocytes using the peptide ligand library technology and advanced mass spectrometry. Molecular & Cellular Proteomics : MCP 7:2254-2269. https://doi.org/10.1074/mcp.M800037-MCP200
  28. Shi ZT, Afzal V, Coller B, Patel D, Chasis JA, Parra M, Lee G, Paszty C, Stevens M, Walensky L, Peters LL, Mohandas N, Rubin E, Conboy JG (1999): Protein 4.1R-deficient mice are viable but have erythroid membrane skeleton abnormalities. The Journal of Clinical Investigation 103:331-340. https://doi.org/10.1172/JCI3858
  29. Steinberg MH (2008) Sickle cell anemia, the first molecular disease: overview of molecular etiology, pathophysiology, and therapeutic approaches. The Scientific World Journal 8:1295-1324. https://doi.org/10.1100/tsw.2008.157
  30. Tilly JL, Kowalski KI, Johnson AL, Hsueh AJ (1991): Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 129: 2799-2801. https://doi.org/10.1210/endo-129-5-2799
  31. Tsantes AE, Bonovas S, Travlou A, Sitaras NM (2006): Redox imbalance, macrocytosis, and RBC homeostasis. Antioxidants & Redox Signaling 8:1205-1216. https://doi.org/10.1089/ars.2006.8.1205
  32. Wang S, Huang W, Shi H, Lin C, Xie M, Wang J (2010): Localization and expression of peroxiredoxin II in the mouse ovary, oviduct, uterus, and preimplantation embryo. Anatomical Record 293:291-297. https://doi.org/10.1002/ar.21031
  33. Watabe S, Hasegawa H, Takimoto K, Yamamoto Y, Takahashi SY (1995): Possible function of SP-22, a substrate of mitochondrial ATP-dependent protease, as a radical scavenger. Biochem Biophys Res Commun 213:1010-1016. https://doi.org/10.1006/bbrc.1995.2229
  34. Wood ZA, Schroder E, Robin Harris J, Poole LB (2003): Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28:32-40. https://doi.org/10.1016/S0968-0004(02)00003-8
  35. Xu D, Suenaga N, Edelmann MJ, Fridman R, Muschel RJ, Kessler BM (2008): Novel MMP-9 substrates in cancer cells revealed by a label-free quantitative proteomics approach. Molecular & Cellular Proteomics : MCP 7:2215-2228. https://doi.org/10.1074/mcp.M800095-MCP200
  36. Xu GW, Ali M, Wood TE, Wong D, Maclean N, Wang X, Gronda M, Skrtic M, Li X, Hurren R, Mao X, Venkatesan M, Beheshti Zavareh R, Ketela T, Reed JC, Rose D, Moffat J, Batey RA, Dhe-Paganon S, Schimmer AD (2010): The ubiquitin-activating enzyme E1 as a therapeutic target for the treatment of leukemia and multiple myeloma. Blood 115: 2251-2259. https://doi.org/10.1182/blood-2009-07-231191
  37. Yang HY, Kwon J, Choi HI, Park SH, Yang U, Park HR, Ren L, Chung KJ, Kim YU, Park BJ, Jeong SH, Lee TH (2012) In-depth analysis of cysteine oxidation by the RBC proteome: advantage of peroxiredoxin II knockout mice. Proteomics 12:101-112. https://doi.org/10.1002/pmic.201100275
  38. Yang S, Luo A, Hao X, Lai Z, Ding T, Ma X, Mayinuer M, Shen W, Wang X, Lu Y, Ma D, Wang S (2011): Peroxiredoxin 2 inhibits granulosa cell apoptosis during follicle atresia through the NFKB pathway in mice. Biology of Reproduction 84:1182-1189. https://doi.org/10.1095/biolreprod.110.087569