Testosterone-dependent sex differences in red blood cell hemolysis in storage, stress, and disease

Transfusion

Volumn 56, Issue 10, 2016, Pages 2571-2583

  Kanias, Tamir ^a,b   Sinchar, Derek ^a   Osei Hwedieh, David ^a   Baust, Jeffrey J ^a   Jordan, Andrew ^c,d   Zimring, James C ^e   Waterman, Hayley R ^e   de Wolski, Karen S ^e   Acker, Jason P ^c,d   Gladwin, Mark T ^a,b  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

^d CANADIAN BLOOD SERVICES   (Canada)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TESTOSTERONE;

ADULT; AGED; ANIMAL MODEL; ARTICLE; BLOOD STORAGE; CHILD; CONTROLLED STUDY; FEMALE; GENETIC PREDISPOSITION; HEMOLYSIS; HUMAN; INFANT; MALE; MOUSE; NEWBORN; NONHUMAN; ORCHIECTOMY; OSMOTIC STRESS; OXIDATIVE STRESS; PRIORITY JOURNAL; SEX DIFFERENCE; AGE; ANIMAL; CANADA; DRUG EFFECTS; ERYTHROCYTE; INBRED MOUSE STRAIN; METABOLISM; MIDDLE AGED; OSMOTIC PRESSURE; UNITED STATES;

ADULT; AGE FACTORS; ANIMALS; BLOOD PRESERVATION; CANADA; ERYTHROCYTES; FEMALE; HEMOLYSIS; HUMANS; MALE; MICE; MICE, INBRED STRAINS; MIDDLE AGED; OSMOTIC PRESSURE; OXIDATIVE STRESS; SEX FACTORS; TESTOSTERONE; UNITED STATES;

EID: 84982947878     PISSN: 00411132     EISSN: 15372995     Source Type: Journal    
DOI: 10.1111/trf.13745     Document Type: Article

References (38)

1. Donadee C, Raat NJ, Kanias T, et al. Nitric oxide scavenging by red blood cell microparticles and cell-free hemoglobin as a mechanism for the red cell storage lesion. Circulation 2011;124:465–76.
2. Alexander JT, El-Ali AM, Newman JL, et al. Red blood cells stored for increasing periods produce progressive impairments in nitric oxide-mediated vasodilation. Transfusion 2013;53:2619–28.
3. Roback JD, Neuman RB, Quyyumi A, et al. Insufficient nitric oxide bioavailability: a hypothesis to explain adverse effects of red blood cell transfusion. Transfusion 2011;51:859–66.
4. Wither M, Dzieciatkowska M, Nemkov T, et al. Hemoglobin oxidation at functional amino acid residues during routine storage of red blood cells. Transfusion 2016;56:421–6.
5. Gladwin MT, Kanias T, Kim-Shapiro DB. Hemolysis and cell-free hemoglobin drive an intrinsic mechanism for human disease. J Clin Invest 2012;122:1205–8.
6. Nouraie M, Lee JS, Zhang Y, et al. The relationship between the severity of hemolysis, clinical manifestations and risk of death in 415 patients with sickle cell anemia in the US and Europe. Haematologica 2013;98:464–72.
7. Atichartakarn V, Chuncharunee S, Archararit N, et al. Intravascular hemolysis, vascular endothelial cell activation and thrombophilia in splenectomized patients with hemoglobin E/β-thalassemia disease. Acta Haematol 2014;132:100–7.
8. Berra L, Pinciroli R, Stowell CP, et al. Autologous transfusion of stored red blood cells increases pulmonary artery pressure. Am J Respir Crit Care Med 2014;190:800–7.
9. Risbano MG, Kanias T, Triulzi D, et al. Effects of aged stored autologous red blood cells on human endothelial function. Am J Respir Crit Care Med 2015;192:1223–33.
10. Steiner ME, Ness PM, Assmann SF, et al. Effects of red-cell storage duration on patients undergoing cardiac surgery. N Engl J Med 2015;372:1419–29.
11. Lacroix J, Hebert PC, Fergusson DA, et al. Age of transfused blood in critically ill adults. N Engl J Med 2015;372:1410–8.
12. Jordan A, Chen D, Yi QL, et al. Assessing the influence of component processing and donor characteristics on quality of red cell concentrates using quality control data. Vox Sang 2016;111:8-15.
13. Kanias T, Gladwin MT. Nitric oxide, hemolysis, and the red blood cell storage lesion: interactions between transfusion, donor, and recipient. Transfusion 2012;52:1388–92.
14. Crisostomo PR, Wang M, Wairiuko GM, et al. Brief exposure to exogenous testosterone increases death signaling and adversely affects myocardial function after ischemia. Am J Physiol Regul Integr Comp Physiol 2006;290:R1168–74.
15. Wang M, Baker L, Tsai BM, et al. Sex differences in the myocardial inflammatory response to ischemia-reperfusion injury. Am J Physiol Endocrinol Metab 2005;288:E321–6.
16. Park KM, Kim JI, Ahn Y, et al. Testosterone is responsible for enhanced susceptibility of males to ischemic renal injury. J Biol Chem 2004;279:52282–92.
17. Platt OS, Brambilla DJ, Rosse WF, et al. Mortality in sickle cell disease. Life expectancy and risk factors for early death. N Engl J Med 1994;330:1639–44.
18. Raval JS, Waters JH, Seltsam A, et al. Menopausal status affects the susceptibility of stored RBCs to mechanical stress. Vox Sang 2011;100:418–21.
19. Kameneva MV, Antaki JF, Yeleswarapu KK, et al. Plasma protective effect on red blood cells exposed to mechanical stress. ASAIO J 1997;43:M571.
20. Kameneva MV, Watach MJ, Borovetz HS. Gender difference in rheologic properties of blood and risk of cardiovascular diseases. Clin Hemorheol Microcirc 1999;21:357–63.
21. Kameneva MV, Watach MJ, Borovetz HS. Rheologic dissimilarities in female and male blood: potential link to development of cardiovascular diseases. Adv Exp Med Biol 2003;530:689–96.
22. Acker JP, Hansen AL, Kurach JD, et al. A quality monitoring program for red blood cell components: in vitro quality indicators before and after implementation of semiautomated processing. Transfusion 2014;54:2534–43.
23. Zwart A, van Assendelft OW, Bull BS, et al. Recommendations for reference method for haemoglobinometry in human blood (ICSH standard 1995) and specifications for international haemiglobinocyanide standard (4th edition). J Clin Pathol 1996;49:271.
24. Kanias T, Wang L, Lippert A, et al. Red blood cell endothelial nitric oxide synthase does not modulate red blood cell storage hemolysis. Transfusion 2013;53:981–9.
25. Gilson CR, Kraus TS, Hod EA, et al. A novel mouse model of red blood cell storage and posttransfusion in vivo survival. Transfusion 2009;49:1546–53.
26. Hod EA, Zhang N, Sokol SA, et al. Transfusion of red blood cells after prolonged storage produces harmful effects that are mediated by iron and inflammation. Blood 2010;115:4284–92.
27. Milton JN, Rooks H, Drasar E, et al. Genetic determinants of haemolysis in sickle cell anaemia. Br J Haematol 2013;161:270–8.
28. Zimring JC, Smith N, Stowell SR, et al. Strain-specific red blood cell storage, metabolism, and eicosanoid generation in a mouse model. Transfusion 2014;54:137–48.
29. Pantaleo A, Ferru E, Carta F, et al. Irreversible AE1 tyrosine phosphorylation leads to membrane vesiculation in G6PD deficient red cells. PLoS One 2011;6:e15847.
30. Pászty C, Brion CM, Manci E, et al. Transgenic knockout mice with exclusively human sickle hemoglobin and sickle cell disease. Science 1997;278:876–8.
31. Middelburg RA, Briet E, van der Bom JG. Mortality after transfusions, relation to donor sex. Vox Sang 2011;101:221–9.
32. Desmarets M, Bardiaux L, Benzenine E, et al. Effect of storage time and donor sex of transfused red blood cells on 1-year survival in patients undergoing cardiac surgery: an observational study. Transfusion 2016;56:1213–22.
33. Makino S, Kunimoto K, Muraoka Y, et al. Breeding of a non-obese, diabetic strain of mice. Jikken Dobutsu 1980;29:1–13.
34. Alonso-Alvarez C, Bertrand S, Faivre B, et al. Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc Biol Sci 2007;274:819–25.
35. March BE, Coates V, Biely J. The effects of estrogen and androgen on osmotic fragility and fatty acid composition of erythrocytes in the chicken. Can J Physiol Pharmacol 1966;44:379–87.
36. DeVenuto F, Wilson SM. Distribution of progesterone and its effect on human blood during storage. Transfusion 1976;16:107–12.
37. Whiting KP, Restall CJ, Brain PF. Steroid hormone-induced effects on membrane fluidity and their potential roles in non-genomic mechanisms. Life Sci 2000;67:743–57.
38. Guo W, Bachman E, Vogel J, et al. The effects of short-term and long-term testosterone supplementation on blood viscosity and erythrocyte deformability in healthy adult mice. Endocrinology 2015;156:1623–9.