Protein kinase C mediates caspase 3 activation: A role for erythrocyte morphology changes

Clinical Hemorheology and Microcirculation

Volumn 59, Issue 4, 2015, Pages 345-354

  Carelli Alinovi, Cristiana ^b   Pirolli, Davide ^b   Giardina, Bruno ^b,c   Misiti, Francesco ^a  

^a UNIVERSITY OF CASSINO AND SOUTHERN LAZIO   (Italy)

^b CATHOLIC UNIVERSITY   (Italy)

^c CNR   (Italy)

Author keywords

caspase 3; nitric oxide; phorbol 12 myristate 13 acetate; PKC; RBCs

Indexed keywords

BENZYLOXYCARBONYLASPARTYLGLUTAMYLVALYLASPARTYL FLUOROMETHYL KETONE; CASPASE 3; CHELERYTHRINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; NITRATE; NITRIC ACID DERIVATIVE; NITRIC OXIDE; NITRITE; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ERYTHROCYTE MEMBRANE; ERYTHROCYTE STRUCTURE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; METABOLISM; NORMAL HUMAN; PROTEIN DEGRADATION; CYTOLOGY; ERYTHROCYTE; SIGNAL TRANSDUCTION;

CASPASE 3; ENZYME ACTIVATION; ERYTHROCYTES; HUMANS; NITRIC OXIDE; PROTEIN KINASE C; SIGNAL TRANSDUCTION;

EID: 84929329317     PISSN: 13860291     EISSN: 18758622     Source Type: Journal    
DOI: 10.3233/CH-141845     Document Type: Article

References (41)

1. N.I. Agalakova and G.P. Gusev, Transient activation of protein kinase C contributes to fluoride-induced apoptosis of rat erythrocytes, Toxicol In Vitro 27 (2013), 2335-2341.
2. Z. Al and C.M. Cohen, Phorbol 12-myristate 13-acetate-stimulated phosphorylation of erythrocyte membrane skeletal proteins is blocked by calpain inhibitors: Possible role of protein kinase M, Biochem J 296 (1993), 675-683.
3. L. Belloni-Olivi, M. Annadata, G.W. Goldstein and J.P. Bressler, Phosphorylation of membrane proteins in erythrocytes treated with lead, Biochem J 315 (1996), 401-406.
4. M. Bor-Kucukatay, R.B. Wenby, H.J. Meiselman and O.K. Baskurt, Effects of nitric oxide on red blood cell deformability, Am J Physiol Heart Circ Physiol 284 (2003), 1577-1584.
5. M.E. Clementi, B. Giardina, D. Colucci, A. Galtieri and F. Misiti, Amyloid-beta peptide affects the oxygen dependence of RBC metabolism: A role for caspase 3, Int J Biochem Cell Biol 39 (2007), 727-735.
6. Y.N. Danilov and C.M. Cohen, Wheat germ agglutinin but not concanavalin A modulates protein kinase C-mediated phosphorylation of red cell skeletal proteins, FEBS Lett 257 (1989), 431-434.
7. K. de Jong, M.P. Rettig, P.S. Low and F.A. Kuypers, Protein kinase C activation induces phosphatidylserine exposure on red blood cells, Biochemistry 41 (2002), 12562-12567.
8. S. de Oliveira, A.S. Silva-Herdade and C. Saldanha, Modulation of RBC deformability by PKC activity, Clin Hemorheol Microcirc 39 (2008), 363-373.
9. S. Ficarra, E. Tellone, B. Giardina, R. Scatena, A. Russo, F. Misiti, M.E. Clementi, D. Colucci, E. Bellocco, G. Laganà, D. Barreca and A. Galtieri, Derangement of erythrocytic AE1 in beta-thalassemia by caspase 3: Pathogenic mechanisms and implications in red blood cell senescence, J Membr Biol 228 (2009), 43-49.
10. 2+/calmodulindependent endothelial nitric oxide synthase activity, Circ Res 88 (2001), 68-75.
11. A. George, S. Pushkaran, D.G. Konstantinidis, S. Koochaki, P. Malik, N. Mohandas, Y. Zheng, C.H. Joiner and T.A. Kalfa, RBC NADPH oxidase activity modulated by Rac GTPases, PKC, and plasma cytokines contributes to oxidative stress in sickle cell disease, Blood 121 (2013), 2099-2107.
12. R.B. Govekar and S.M. Zingde, Protein kinase C isoforms in human RBCs, Ann Hematol 80 (2001), 31-534.
13. R.B. Govekar, P.D. Kawle, S.H. Advani, S.M. Zingde and P.K.C. Reduced, α Activity Induces Senescent Phenotype in Erythrocytes, Anemia 2012 (2012), 168050.
14. J.M. Herbert, J.M. Augereau, J. Gleye and J.P. Maffrand, Chelerythrine is a potent and specific inhibitor of protein kinase C, Biochem Biophys Res Commun 172 (1990), 993-999.
15. M. Junco, C. Webster, C. Crawford, L. Bosca and P.J. Parker, Protein kinase C V3 domain mutants with differential sensitivities to m-calpain are not resistant to phorbol-ester-induced down-regulation, Eur J Biochem 223 (1994), 2592-2263.
16. M.M. Kay, G.J. Bosman, S.S. Shapiro, A. Bendich and P.S. Bassel, Oxidation as a possible mechanism of cellular aging: Vitamin E deficiency causes premature aging and IgG binding to RBCs, Proc Natl Acad Sci U S A 83 (1986), 2463-2467.
17. M.M. Kay, S.Z. Rapcsak, G.J. Bosman and J.R. Goodman, Posttranslational modifications of brain and RBC band 3 during aging and disease, Cell Mol Biol (Noisy-le-grand) 42 (1996), 919-944.
18. B.A. Klarl, P.A. Lang, D.S. Kempe, O.M. Niemoeller, A. Akel, M. Sobiesiak, K. Eisele, M. Podolski, S.M. Huber, T. Wieder and F. Lang, Protein kinase C mediates RBC "programmed cell death" following glucose depletion, Am J Physiol Cell Physiol 290 (2006), 244-253.
19. P. Kleinbongard, A. Dejam, T. Lauer, T. Rassaf, A. Schindler, O. Picker, T. Scheeren, A. Gödecke, J. Schrader, R. Schulz, G. Heusch, G.A. Schaub, N.S. Bryan, M. Feelisch and M. Kelm, Plasma nitrite reflects constitutive nitric oxide synthase activity in mammals, Free Radic Biol Med 8 (2003), 790-796.
20. P. Kleinbongard, R. Schulz, T. Rassaf, T. Lauer, A. Dejam, T. Jax, I. Kumara, P. Gharini, S. Kabanova, B. Ozuyaman, H.G. Schnurch, A. Godecke, A.A. Weber, M. Robenek, H. Robenek, W. Bloch, P. Rosen and M. Kelm, Red blood cells express a functional endothelial nitric oxide synthase, Blood 107 (2006), 2943-2951.
21. H. Lenasi, K. Kohlstedt, B. Fichtlscherer, A. Mulsch, R. Busse and I. Fleming, Amlodipine activates the endothelial nitric oxide synthase by altering phosphorylation on Ser1177 and Thr495, Cardiovasc Res 59 (2003), 844-853.
22. Z. Li, J.D. Carter, L.A. Dailey and Y.C. Huang, Vanadyl sulfate inhibits NO production via threonine phosphorylation of eNOS, Environ Health Perspect 112 (2004), 201-206.
23. E. Maellaro, S. Leoncini, D. Moretti, B. Del Bello, I. Tanganelli, C. De Felice and L. Ciccoli, RBC caspase-3 activation and oxidative imbalance in RBCs and in plasma of type 2 diabetic patients, Acta Diabetol 50 (2011), 489-495.
24. D. Mandal, V. Baudin-Creuza, A. Bhattacharyya, S. Pathak, J. Delaunay, M. Kundu and J. Basu, Caspase 3-mediated proteolysis of the N-terminal cytoplasmic domain of the human erythroid anion exchanger 1 (band 3), J Biol Chem 278 (2003), 52551-52558.
25. M. Matsubara, N. Hayashi, T. Jing and K. Titani, Regulation of endothelial nitric oxide synthase by protein kinase C, J Biochem (Tokyo) 133 (2003), 773-781.
26. I. Messana, D.V. Rossetti, F. Misiti, F. Vincenzoni, E. Tellone, B. Giardina and M. Castagnola, Determination of S-nitrosoglutathione in RBCs by capillary zone electrophoresis, Electrophoresis 21 (2000), 1606-1610.
27. B.J. Michell, Z. Chen, T. Tiganis, D. Stapleton, F. Katsis, D.A. Power, A.T. Sim and B.E. Kemp, Coordinated control of endothelial nitric oxide synthase phosphorylation by protein kinase C and the cAMP-dependent protein kinase, J Biol Chem 276 (2001), 17625-17628.
28. Y. Miki, T. Tazawa, K. Hirano, H. Matsushima, S. Kumamoto, N. Hamasaki, T. Yamaguchi and M. Beppu, Clearance of oxidized RBCs by macrophages: Involvement of caspases in the generation of clearance signal at band 3 glycoprotein, Biochem Biophys Res Commun 363 (2007), 57-62.
29. F. Misiti, F. Orsini, M.E. Clementi, D. Masala, E. Tellone, A. Galtieri and B. Giardina, Amyloid peptide inhibits ATP release from human RBCs, Biochem Cell Biol 86 (2008), 501-508.
30. F. Misiti, C. Carelli-Alinovi, B. Sampaolese and B. Giardina, β-amyloid decreases detectable endothelial nitric oxide synthase in human RBCs: A role for membrane acetylcholinesterase, Cell Biochem Funct 30 (2012), 474-479.
31. A.V. Muravyov and I.A. Tikhomirova, Role molecular signaling pathways in changes of red blood cell deformability, Clin Hemorheol Microcirc 53 (2013), 45-59.
32. M. Nakagawa, J.L. Oliva, D. Kothapalli, A. Fournier, R.K. Assoian and M.G. Kazanietz, Phorbol ester-induced G1 phase arrest selectively mediated by protein kinase Cδ-dependent induction of p21, J Biol Chem 280 (2005), 33926-33934.
33. J.P. Nicolay, G. Liebig, O.M. Niemoeller, S. Koka, M. Ghashghaeinia, T. Wiede, J. Haendeler, R. Busse and F. Lang, Inhibition of suicidal RBC death by nitric oxide, Pflugers Arch 456 (2008), 293-305.
34. E. Oskoueian, N. Abdullah and S. Ahmad, Phorbol esters from Jatropha meal triggered apoptosis, activated PKC-δ, caspase-3 proteins and down-regulated the proto-oncogenes in MCF-7 and HeLa cancer cell lines, Molecules 17 (2012), 10816-10830.
35. B. Ozüyaman, M. Grau, M. Kelm, M.W. Merx and P. Kleinbongard, RBC NOS: Regulatory mechanisms and therapeutic aspects, Trends Mol Med 14 (2008), 314-322.
36. I.C. Park, M.J. Park, C.H. Rhee, J.I. Lee, T.B. Choe, J.J. Jang, S.H. Lee and S.I. Hong, Protein kinase C activation by PMA rapidly induces apoptosis through caspase-3/CPP32 and serine protease(s) in a gastric cancer cell line, Int J Oncol 18 (2001), 1077-10783.
37. C. Partovian, Z. Zhuang, K. Moodie, M. Lin, N. Ouchi, W.C. Sessa, K. Walsh and M. Simons, PKC alpha activates eNOS and increases arterial blood flow in vivo, Circ Res 97 (2005), 482-487.
38. D. Pietraforte, P. Matarrese, E. Straface, L. Gambardella, A. Metere, G. Scorza, T.L. Leto, W. Malorni and M. Minetti, Two different pathways are involved in peroxynitrite-induced senescence and apoptosis of human RBCs, Free Radic Biol Med 42 (2007), 202-214.
39. M.E. Reyland, S.M. Anderson, A.A. Matassa, K.A. Barzen and D.O. Quissell, Protein kinase C delta is essential for etoposide-induced apoptosis in salivary gland acinar cells, J Biol Chem 274 (1999), 19115-19123.
40. A.S. Silva-Herdade, T. Freitas, J.P. Almeida and C. Saldanha, Erythrocyte deformability and nitric oxide mobilization under pannexin-1 and PKC dependence. Clin Hemorheol Microcirc (2014), DOI: 10.3233/CH-141833.
41. Y. Suzuki, N. Ohkubo, M. Aoto, N. Maeda, I. Cicha, T. Miki and N., Mitsuda, Participation of caspase-3-like protease in oxidation-induced impairment of RBC membrane propertie, Biorheology 44 (2007), 179-190.