Abstract
Background:
Erythrocyte swelling in non-ionic sucrose media and the subsequent osmotic lysis are influenced by mechanisms of regulatory volume adjustment and osmotic water permeability. Kinetics of transmembrane water and ion fluxes in varied physiologic states may determine the phenotype of erythrocyte osmotic fragility (EOF) and affect estimates of EOF.
Methods:
Effects of sex, age, late pregnancy (third trimester) and lactation on the haemolysis of Sahel goat erythrocytes incubated in a series of hyposmotic non-ionic sucrose media were investigated.
Results:
The fragiligram was sigmoidal in 72 (97%) out of 74 goats. Two male (3%) goats with low and high extreme median erythrocyte fragilities (MEF), had non-sigmoidal curves. The mean fragilities at osmolarities of 30–300 mosmol/L of sucrose and the mean osmolarities responsible for 10%–90% haemolysis (CH10–CH90) were not significantly different between males and non-pregnant dry (NPD) females, amongst the age groups and between pregnant or lactating and NPD female goats. The MEF (CH50) of the goats were at osmolarities of 126–252 mosmol/L (median of data: 171 mosmol/L) with a mean of 175.24±16.20 mosmol/L. Therefore, phenotypic homogeneity of EOF occurred with minor deviance, since EOF variables were not differentiated by sex, age, late pregnancy or lactation.
Conclusions:
Physiologic states of the goat did not affect EOF phenotype in non-ionic sucrose media. Sigmoidal fragility phenotype seemed to be homogeneously conserved by osmoregulatory mechanisms not partitioned by sex, age, late pregnancy or lactation, but a minor non-sigmoidal curve might have occurred due to altered erythrocyte osmotic behaviour that would require further investigation.
Acknowledgments
Ismaila Gadaka, Chima V. Maduka, Alapa B. Ikpe and Sylvester Ogbaji provided technical and material assistance. We wish to thank the management of the University Farm for allowing us to study the goats on the farm.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in writing of the report; or in the decision to submit the report for publication.
References
1. Parpart AK, Loenz PB, Parpart ER, Gregg JR, Chase AM. The osmotic resistance (fragility) of human red cells. J Clin Invest 1947;26:636–40.10.1172/JCI101847Search in Google Scholar
2. Gottfried EL, Robertson NA. Glycerol lysis time as a screening test for erythrocyte disorders. J Lab Clin Med 1974;83:323–33.Search in Google Scholar
3. Zanella A, Izzo C, Rebulla P, Zanuso F, Perroni L, Sirchia G. Acidified glycerol lysis test: a screening test for spherocytosis. Br J Haematol 1980;45:481–6.10.1111/j.1365-2141.1980.tb07167.xSearch in Google Scholar
4. Jenkins DE Jr, Hartmann RC, Kerns AL. Serum-red cell interactions at low ionic strength: erythrocyte complement coating and hemolysis of paroxysmal nocturnal hemoglobinuria. J Clin Invest 1967;46:753–61.10.1172/JCI105576Search in Google Scholar
5. Igbokwe NA, Igbokwe IO. Influence of extracellular media’s ionic strength on the osmotic stability of Sahel goat erythrocytes. J Basic Clin Physiol Pharmacol 2015;26:171–9.10.1515/jbcpp-2014-0014Search in Google Scholar
6. March BE, Coates V, Biely J. The effects of estrogen and androgen on osmotic fragility and fatty acid composition of erythrocyte in the chicken. Can J Physiol Pharmacol 1966;44:379–87.10.1139/y66-045Search in Google Scholar
7. Olayemi FO. The effect of sex on the erythrocyte osmotic fragility of the Nigerian White Fulani and Ndama breeds of cattle. Top Vet 2007;25:106–11.Search in Google Scholar
8. Oyewale JO, Ajibade HA. The osmotic fragility of erythrocytes of turkeys of two age groups. Vet Arhiv 1990;60:43–8.Search in Google Scholar
9. Oyewale JO. Osmotic fragility of erythrocytes of guinea-fowls at 21 and 156 weeks of age. Vet Arhiv 1991;61:49–56.Search in Google Scholar
10. Penha-Silva N, Firmino BC, Reis FG, Huss JC, Souza TM, de Freitas MV, et al. Influence of age on the stability of human erythrocyte membranes. Mech Ageing Dev 2007;128:444–9.10.1016/j.mad.2007.06.007Search in Google Scholar
11. Igbokwe NA, Ojo NA, Igbokwe IO. Effects of sex and age on the osmotic stability of Sahel goat erythrocytes. Comp Clin Pathol 2016;25:15–22.10.1007/s00580-015-2130-zSearch in Google Scholar
12. Magid MS, Perlin M, Gottfried EL. Increased erythrocyte osmotic fragility in pregnancy. Am J Obstet Gynecol 1982;44:910–4.10.1016/0002-9378(82)90183-1Search in Google Scholar
13. Arora B, Punia RS, Lal P, Arora DR. The effect of pregnancy on erythrocyte osmotic fragility. J Nepal Med Assoc 1994;32: 227–30.10.31729/jnma.1264Search in Google Scholar
14. Habibu B, Kawu MU, Makun HJ, Aluwong T, Yaqub LS, Ahmad MS, et al. Influence of sex, reproductive status and foetal number on erythrocyte osmotic fragility, haematological and physiological parameters in goats during the hot-dry season. Vet Med Czech 2014;59:479–90.10.17221/7778-VETMEDSearch in Google Scholar
15. Igbokwe NA, Ojo NA, Igbokwe IO. Quantified effects of late pregnancy and lactation on the osmotic stability of Sahel goat erythrocytes. Nig Vet J 2015;32:1122–9.Search in Google Scholar
16. Durotoye LA. The effect of sex, pregnancy and lactation on the osmotic fragility of the West African dwarf sheep. Bull Anim Hlth Prod Afr 1987;35:29–33.Search in Google Scholar
17. Lijnen N, Petrov V. Cholesterol modulation of transmembrane cation transport systems in human erythrocytes. Biochem Mol Med 1995;56:52–62.10.1006/bmme.1995.1056Search in Google Scholar
18. Bruckdorfer KR, Demel RA, De Gier J, van Deenen LL. The effect of partial replacements of membrane cholesterol by other steroids on the osmotic fragility and glycerol permeability of erythrocytes. Biochim Biophys Acta 1969;183:334–45.10.1016/0005-2736(69)90089-3Search in Google Scholar
19. Sagawa S, Shiraki K. Changes of osmotic fragility of red blood cells due to repletion or depletion of cholesterol in human and rat red cells in vitro. J Nutr Sci Vitaminol (Tokyo) 1980;26:161–9.10.3177/jnsv.26.161Search in Google Scholar
20. Horii K, Adachi Y, Ohba Y, Yamamoto T. Erythrocyte osmotic fragility in various liver disease-application of coil planet centrifuge system. Gasteroenterol Jpn 1981;16:161–7.10.1007/BF02774390Search in Google Scholar
21. Igbokwe NA, Ojo NA, Igbokwe IO. Phenotypic drift in osmotic fragility of Sahel goat erythrocytes associated with variability of median fragility. Sokoto J Vet Sci 2015;13:6–13.10.4314/sokjvs.v13i2.2Search in Google Scholar
22. Igbokwe NA, Igbokwe IO. Phenotypic variations in osmotic lysis of Sahel goat erythrocytes in non-ionic glucose media. J Basic Clin Physiol Pharmacol 2016;27:147–54.10.1515/jbcpp-2015-0036Search in Google Scholar
23. Schalm OW, Jain NC, Carroll EJ. Veterinary hematology, 3rd ed. Philadelphia: Lea and Fabiger, 1975.Search in Google Scholar
24. Glaji YA, Mani AU, Igbokwe IO. Relationship of faecal egg count with packed cell volume and anaemia in Sahel sheep and goats in semi-arid northeastern Nigeria. Comp Clin Pathol 2014;23:1195–201.10.1007/s00580-013-1762-0Search in Google Scholar
25. Waziri MA, Ribadu AY, Sivachelvan N. Changes in the serum proteins, hematological and some serum biochemical profiles in the gestation period in the Sahel goat. Vet Arhiv 2010;80:215–24.Search in Google Scholar
26. Hoffmann K, Dunham PB. Membrane mechanisms and intracellular signalling in cell volume regulation. Int Rev Cytol 1995;161:173–262.10.1016/S0074-7696(08)62498-5Search in Google Scholar
27. Lang F, Busch GL, Ritter M, Völkl H, Waldegger S, Gulbins E, et al. Functional significance of cell volume regulatory mechanisms. Physiol Rev 1998;78:247–306.10.1152/physrev.1998.78.1.247Search in Google Scholar PubMed
28. Dewey MJ, Brown JL, Nallaseth FS. Genetic differences in red cell osmotic fragility: analysis in allophonic mice. Blood 1982;59:986–9.10.1182/blood.V59.5.986.986Search in Google Scholar
29. Schaefer CA, Dewy MJ. Single locus (rol) control of extreme resistance to red cell osmotic lysis: intrinsic mode of gene action. Genetics 1989;121:353–8.10.1093/genetics/121.2.353Search in Google Scholar
30. Armsby CC, Stuart-Tilley AK, Alper SL, Brugnara C. Resistance to osmotic lysis in BXD-31 mouse erythrocytes: association with upregulated K-Cl cotransport. Am J Physiol 1996;270:C866–77.10.1152/ajpcell.1996.270.3.C866Search in Google Scholar
31. Pieragostini E, Petazzi F, Luccia AD. The relationship between the presence of extra α-globin gene and blood cell traits in Altamurana sheep. Genet Select Evol 2003;35(Suppl 1):S121–33.10.1186/1297-9686-35-S1-S121Search in Google Scholar
32. Cossins AR, Gibson JS. Volume-sensitive transport systems and volume homeostasis in vertebrate red blood cells. J Exp Biol 1997;200:343–52.10.1242/jeb.200.2.343Search in Google Scholar
33. Day RE, Kitchen P, Owen DS, Bland C, Marshall L, Conner AC, et al. Human aquaporins: Regulators of transcellular water flow. Biochim Biophys Acta 2014;1840:1492–506.10.1016/j.bbagen.2013.09.033Search in Google Scholar
34. Mola MG, Sparaneo A, Gargano CD, Spray DC, Svelto M, Frigeri A, et al. The speed of swelling kinetics modulates cell volume regulation and calcium signalling in astrocytes: A different point of view on the role of aquaporin. Glia 2016;64:139–54.10.1002/glia.22921Search in Google Scholar
35. Nageltius EA, Mathiisen TM, Ottersen OP. Aquaporin-4 in the central nervous system: cellular and subcellular distribution and coexpression with KIR4.1. Neurosci 2004;129:905–13.10.1016/j.neuroscience.2004.08.053Search in Google Scholar
36. Liu X, Bandyopadhyay BB, Nakamoto T, Singh BB, Liedtke W, Melvin JE, et al. A role for AQP5 in activation of TRPV4 by hypotonicity: concerted involvement of AQP5 and TRPV4 in regulation of cell volume recovery. J Biol Chem 2006;281:15485–95.10.1074/jbc.M600549200Search in Google Scholar
37. Rungaldier S, Oberwagner W, Salzer U, Csasza E, Prohaska R. Stomatin interacts with GLUT/SLC 2A1, band 3/SLC 4A1, and aquaporin-1 in human erythrocyte membrane domains. Biochim Biophys Acta 2013;1828:956–66.10.1016/j.bbamem.2012.11.030Search in Google Scholar
38. Daniel G. Functional aspects of red cell antigens. Blood Rev 1999;13;14–35.10.1016/S0268-960X(99)90020-6Search in Google Scholar
39. Preston GM, Smith BL, Zeidel ML, Moulds JJ, Agre P. Mutations in aquaporin-1 in phenotypically normal humans without functional CHIP water channels. Science 1994;265:1585–7.10.1126/science.7521540Search in Google Scholar PubMed
40. Mathia JC, Mori S, Smith BL, Preston GM, Mohandas N, Collin M, et al. Functional analysis of aquaporin-1 deficient red cells. The colton-null phenotype. J Biol Chem 1996;271:1309–13.10.1074/jbc.271.3.1309Search in Google Scholar PubMed
41. Ma T, Yang B, Verkman AS. Low osmotic water permeability in erythrocytes from transgenic mice lacking water channel aquaporin-1. Biophys J 1998;74:A394–4 Th-Pos 279.Search in Google Scholar
42. Yang B, Ma T, Verkman AS. Erythrocyte water permeability and renal function in double knockout mice lacking aquaporin-1 and aquaporins-3. J Biol Chem 2001;276:624–8.10.1074/jbc.M008664200Search in Google Scholar PubMed
43. Yan Y, Huang J, Ding F, Mei J, Zhu J, Liu H, et al. Aquaporin 1 plays an important role in myocardial edema caused by cardiopulmonary bypass surgery in goat. Int J Mol Med 2013;31: 637–43.10.3892/ijmm.2013.1228Search in Google Scholar PubMed
44. Ding FB, Yan YM, Huang JB, Mei J, Zhu JQ, Liu H. The involvement of AQP1 in heart oedema induced by global myocardial ischemia. Cell Biochem Funct 2013;31:60–4.10.1002/cbf.2860Search in Google Scholar PubMed
45. Elfers K, Breves G, Muscher-Banse AS. Modulation of auaporin 2 expression in the kidney of young goats by changes in nitrogen intake. J Comp Physiol B 2014;184:929–36.10.1007/s00360-014-0849-5Search in Google Scholar PubMed
46. Stewart AK, Shmukler BE, Vandrope DH, Rivera A, Heneghan JF, Li X, et al. Loss-of-function and gain-of-function phenotypes of stomatocytosis mutant RhAG F65S. Am J Physiol Cell Physiol 2011;301:C1325–43.10.1152/ajpcell.00054.2011Search in Google Scholar PubMed PubMed Central
47. Nagasawa T. Deformability and osmotic fragility of phenylhydrazine-injected rat erythrocytes fractionated by percoll density-gradient. Jpn J Physiol 1982;32:161–71.10.2170/jjphysiol.32.161Search in Google Scholar PubMed
48. Olusanya SK, Adepoju FO. Osmotic fragility of erythrocyte of some Nigerian species of domestic ruminants. Bull Anim Hlth Prod Afr 1979;27:237–43.Search in Google Scholar
49. Quarmyne MO, Risinger M, Linkgel A, Frazier A, Joiner C. Volume regulation and KCl cotransport in reticulocyte populations of sickle and normal red blood cells. Blood Cell Mol Dis 2011;47:95–9.10.1016/j.bcmd.2011.04.007Search in Google Scholar PubMed PubMed Central
50. Rust MB, Alper SL, Rudhard Y, Smukler BE, Vicente R, Brugnara C, et al. Disruption of erythroid K-Cl cotransporters alters erythrocyte volume and partially rescues erythrocyte dehydration in SAD mice. J Clin Invest 2007;117:1708–17.10.1172/JCI30630Search in Google Scholar PubMed PubMed Central
Supplemental Material:
The online version of this article (DOI: 10.1515/jbcpp-2016-0004) offers supplementary material, available to authorized users.
©2016 Walter de Gruyter GmbH, Berlin/Boston
