Òðîìáîç, ãåìîñòàç è ðåîëîãèÿ. — 2013. — ¹3(55). — Ñ. 4.

Îáçîð

ÓÄÊ 612.11/13:612.111/117.2

ÄÅÔÎÐÌÈÐÓÅÌÎÑÒÜ ÝÐÈÒÐÎÖÈÒÎÂ: ÎÑÍÎÂÍÛÅ ÌÅÕÀÍÈÇÌÛ ÑÐÎ×ÍÎÉ ÀÄÀÏÒÀÖÈÈ

À. Â. Ìóðàâüåâ ¹, Å. Â. Ðîéòìàí ², È. À. Òèõîìèðîâà ¹, À. À. Ìóðàâüåâ ¹, Ñ. Â. Áóëàåâà ¹, Ï. Â. Ìèõàéëîâ ¹

ÔÃÁÎÓ ÂÏÎ ßðîñëàâñêèé ãîñóäàðñòâåííûé ïåäàãîãè÷åñêèé óíèâåðñèòåò èì. Ê. Ä. Óøèíñêîãî ¹, ßðîñëàâëü;
ÔÃÁÓ Ôåäåðàëüíûé íàó÷íî-êëèíè÷åñêèé öåíòð äåòñêîé ãåìàòîëîãèè, îíêîëîãèè è èììóíîëîãèè èìåíè Äìèòðèÿ Ðîãà÷åâà Ìèíçäðàâñîöðàçâèòèÿ Ðîññèéñêîé Ôåäåðàöèè ²; Ìîñêâà, Ðîññèÿ

Âûïîëíåí îáçîð îñíîâíûõ ýêñïåðèìåíòàëüíûõ è òåîðåòè÷åñêèõ èññëåäîâàíèé âàæíîé ìèêðîðåîëîãè÷åñêîé õàðàêòåðèñòèêè ýðèòðîöèòîâ — èõ äåôîðìèðóåìîñòè. Îáñóæäåíà ðîëü äåôîðìàöèè ýðèòðîöèòîâ â òðàíñïîðòå êèñëîðîäà è îêñèãåíàöèè òêàíåé íà óðîâíå êðóïíûõ ñîñóäîâ è â ñèñòåìå ìèêðîöèðêóëÿöèè. Èññëåäîâàíà ðîëü ìåìáðàííûõ áåëêîâ â äåôîðìàöèè ýðèòðîöèòîâ; ïîêàçàíû ïîñëåäñòâèÿ èõ ôîñôîðèëèðîâàíèÿ ðàçíûìè ïðîòåèíêèíàçàìè ïðè ñðî÷íîé àäàïòàöèè ýðèòðîöèòîâ ê ìåíÿþùèìñÿ çàïðîñàì òêàíåâîãî ìåòàáîëèçìà. Âûïîëíåí àíàëèç ðàçíûõ ýëåìåíòîâ ìîëåêóëÿðíûõ ñèãíàëüíûõ êàñêàäîâ, ñâÿçàííûõ ñ èçìåíåíèåì ýòîé ñóùåñòâåííîé ìèêðîðåîëîãè÷åñêîé õàðàêòåðèñòèêè ýðèòðîöèòîâ. Ïîêàçàíà âàæíàÿ ðîëü ýðèòðîöèòîâ êàê ñåíñîðîâ ãèïîêñèè è ó÷àñòèå èõ â ðåãóëÿöèè òîíóñà àðòåðèîë ïóòåì âûäåëåíèÿ ðåãóëÿòîðíîé ìîëåêóëû — àäåíîçèíòðèôîñôàòà.

Êëþ÷åâûå ñëîâà: ýðèòðîöèòû — äåôîðìèðóåìîñòü — ìèêðîöèðêóëÿöèÿ — ñèãíàëüíûå ìîëåêóëû.

ÄËß ÊÎÐÐÅÑÏÎÍÄÅÍÖÈÈ
Ìóðàâü¸â Àëåêñåé Âàñèëüåâè÷ — ä. á. í., ïðîôåññîð ÔÃÁÎÓ ÂÏÎ ßÃÏÓ èì. Ê. Ä. Óøèíñêîãî.
Àäðåñ: 150000, Ðîññèÿ, ßðîñëàâëü, Ðåñïóáëèêàíñêàÿ óëèöà, ä. 108.
E-mail: alexei.47@mail.ru

Ñòàòüÿ ïîñòóïèëà 27.08.2012, ïðèíÿòà ê ïå÷àòè 30.11.2012.

ERYTHROCYTES DEFORMABILITY: BASIC MECHANISMS OF SHORTM ADAPTATION

A. V. Muravyov ¹, E. V. Roitman ², I. A. Tikhomirova ¹, A. A. Muravyov ¹, S. V. Bulaeva ¹, P. V. Mikhailov ¹

Yaroslavl State Pedagogical University named after K. D. Ushinsky ¹, Yaroslavl; Federal Research Center of Pediatric Hematology, Oncology and Immunology named after Dmitry Rogachev, Ministry of Public Health and Social Development of Russian Federation ²; Moscow; Russia

A review of basic experimental and theoretical studies of important microrheological erythrocytes characteristics — their deformability is presented and its role in oxygen transport and tissue oxygenation in macro- and microcirculation is discussed. The role of membrane proteins in erythrocytes deformation is studied; eff ects of their phosphorylation by diff erent protein kinases in short-term erythrocytes adaptation to tissue oxygen demands are shown. The analysis of diff erent molecular signaling cascades associated with erythrocytes deformability is completed. The important role of erythrocytes as hypoxia sensor and regulator of arterioles tone by means of adenosine triphosphate is shown.

Key words: erythrocytes — deformability — microcirculation — signal molecules.

Ëèòåðàòóðà/References

1. Äæîíñîí Ï. Ïåðèôåðè÷åñêîå êðîâîîáðàùåíèå [Ïåð. ñ àíãë.]. — Ì.: Ìåäèöèíà, 1982. — 396 ñ.
2. Cokelet G. B., Meiselman H. J. Rheological comparison of hemoglobin solutions and erythrocyte suspensions // Science. — 1968. — Vol. 162. — P. 275–277.
3. Óèëêèíñîí Ó. Ë. Íåíüþòîíîâñêèå æèäêîñòè [Ïåð. ñ àíãë.]. — Ì.: Ìèð, 1964. — 216 ñ.
4. Ìóðàâüåâ À. Â., ×åïîðîâ Ñ. Â. Ãåìîðåîëîãèÿ (ýêñïåðè- ìåíòàëüíûå è êëèíè÷åñêèå àñïåêòû ðåîëîãèè êðîâè): Ìîíîãðàôèÿ. — ßðîñëàâëü: Èçä-âî ßÃÏÓ èì. Ê. Ä. Óøèí- ñêîãî, 2009. — 178 ñ.
5. Chasis J. A., Mohandas N. Erythrocyte membrane deformability and stability: two distinct membrane properties that are independently regulated by skeletal protein as sociations // J. Cell. Biol. — 1986. — Vol. 103. — P. 343–350.
6. Arduini A., Rossi M., Mancinelli G. at al. Eff ect of L-carnitine and acetyl-L-carnitine on the human erythrocyte membrane stability and deformability // Life Sci. — 1990. — Vol. 47. — P. 2395–2400.
7. Nunomura W., Takakuwa Y. Regulation of protein 4.1R interactions with membrane proteins by Ca 2+ and calmodulin // Front Biosci. — 2006. — Vol. 11. — P. 1522–1539.
8. Stoltz J. F., Donner M. Red blood cell aggregation: measurements and clinical applications // Turkish J. Med. Sci. — 1991. — Vol. 15. — P. 26–39.
9. Baskurt O. K., Meiselman H. J. Blood rheology and hemodynamics // Semin. Thromb. Hemost. — 2003. — Vol. 29, ¹ 5. — P. 435–450.
10. Minetti G., Ciana A., Balduini C. Diff erential sorting of tyrosine kinases and phosphotyrosine phosphatases acting on band 3 during vesiculation of human erythrocytes // Biochem. J. — 2004. — Vol. 377 (Pt 2). — P. 489–497.
11. Cooke B. M., Lim C. T. Mechanical and adhesive properties of healthy and diseased red blood cells. — Handbook of Hemorheology and Hemodynamics. — Amsterdam: IOS Press, 2007. — 455 ð.
12. Êóïðèÿíîâ Â. Â., Êàðàãàíîâ ß. Ë., Êîçëîâ Â. È. Ìèêðî- öèðêóëÿòîðíîå ðóñëî. — Ì.: Ìåäèöèíà, 1975. — 216 ñ.
13. ×åðíóõ À. Ì., Àëåêñàíäðîâ Ï. Í., Àëåêñååâ Î. Â. Ìèêðî- öèðêóëÿöèÿ. — Ì.: Ìåäèöèíà, 1975. — 455 ñ.
14. Mohandas N. Molecular bases for red cell membrane viscoelastic properties // Biochim. Soc. Trans. — 1992. — Vol. 20. — P. 776–782.
15. Berga L., Dolz J., Vives-Corrons J.L. et al. Viscometric methods for assessing red cell deformability and fragmentation // Biorheology Suppl. — 1984. — Vol. 1. — P. 297–301.
16. Stuart J., Nash G. B. Red cell deformability and haematological disorders // Blood Rev. — 1990. — Vol. 4, ¹ 3. — P. 141–147.
17. Manno S., Takakuwa Y., Mohandas N. Modulation of erythrocyte membrane mechanical function by protein 4.1 phosphorylation // J. Biol. Chem. — 2005. — Vol. 280, ¹ 9. — Ð. 7581–7587.
18. Nash G. B., Meiselman H. J. Red cell and ghost viscoelasticity. Eff ects of hemoglobin concentration and in vivo aging // Biophys. J. — 1983. — Vol. 43, ¹ 1. — P. 63–73.
19. Pfaff erott C., Nash G. B., Meiselman H. J. Red blood cell deformation in shear fl ow. Eff ects of internal and external phase viscosity and of in vivo aging // Biophys. J. — 1985. — Vol. 47, ¹ 5. — P. 695–704.
20. Kon K., Maeda N., Shiga T. Erythrocyte deformation in shear fl ow: infl uences of internal viscosity, membrane stiff ness, and hematocrit // Blood. — 1987. — Vol. 69. — P. 727–734.
21. Drochon A., Barthes-Biesel D., Lacombe C., Lelievre J. C. Determination of the red blood cell apparent membrane elastic modulus from viscometric measurements // J. Biomech. Eng. — 1990. — Vol. 112. — P. 241–249.
22. Burton A. C. Role of geometry of size and shape in microcirculation // Fed. Prpc. — 1966. — Vol. 25. — P. 1753–1760.
23. Èâåíñ È., Ñêåéëàê Ð. Ìåõàíèêà è òåðìîäèíàìèêà áèîëî- ãè÷åñêèõ ìåìáðàí [Ïåð. ñ àíãë.]. — Ì.: Ìèð, 1982. — 304 ñ.
24. Evans E. A. Structure and deformation properties of red blood cells: concepts and quantitative methods // Methods Enzymol. — 1989. — Vol. 173. — P. 3–35.
25. Neu B., Sowemimo-Coker S.O., Meiselman H. J. Cell-cell affi nity of senescent human erythrocytes // Biophys J. — 2003. — Vol. 85, ¹ 1. — P. 75–84.
26. Dintenfass L. Theoretical aspects and clinical applications of the blood viscosity equation containing a term for the internal viscosity of the red cell // Blood Cells. — 1977. — Vol. 3, ¹ 2. — P. 367–374.
27. Schmid-Sch"onbein H., Gaehtgens P. What is red cell deformability? // Scand. J. Clin. Lab. Invest. Suppl. — 1981. — Vol. 41 (Suppl 156). — P. 13–26.
28. Evans E.A, Hochmuth R. M. A solid-liquid composite model of the red cell membrane // J. Membr. Biol. — 1977. — Vol. 30, ¹ 4. — P. 351–362.
29. Takakuwa Y., Mohandas N., Ishibashi T. Regulation of red cell membrane deformability and stability by skeletal protein network // Biorheology. — 1990. — Vol. 27, ¹ 3–4. — P. 357–365.
30. Mohandas N., Chasis J. A. Red blood cell deformability, membrane material properties and shape: regulation by transmembrane, skeletal and cytosolic proteins and lipids // Semin. Hematol. — 1993. — Vol. 30, ¹ 3. — P. 171–192.
31. Chien S., Sung L. P. Molecular basis of red cell membrane rheology. Part 1 // Biorheology. — 1990. — Vol. 27, ¹ 3–4. — P. 327–344.
32. Sridharan M., Bowles E. A., Richards J. P. et al. Prostacyclin receptor-mediated ATP release from erythrocytes requires the voltage-dependent anion channel // Am. J. Physiol. Heart. Circ. Physiol. — 2012. — Vol. 302, ¹ 3. — H553-Í559.
33. Pasini E. M., Kirkedaard M., Salerno D. et al. Deep coverage mouse red blood cell proteome. A fi rst comparison with the human red blood cell // Mol. Cell. Proteomics. — 2008. — Vol. 7. — P. 1317–1330.
34. Cohen C. M., Foley S. F. Biochemical characterization of complex formation by human erythrocyte spectrin, protein 4.1 and actin // Biochemistry. — 1984. — Vol. 23. — P. 6091–6098.
35. Stromqvist M., Backman L., Shanbhag V. P. Eff ect of spectrin dimer on actin polymerization // FEBS Lett. — 1985. — Vol. 190, ¹ 1. — Ð. 15–20.
36. Anderson J. P., Morrow J. S. The interaction of calmodulin with human erythrocyte spectrin. Inhibition of protein 4.1-stimulated actin binding // J. Biol. Chem. — 1987. — Vol. 262, ¹ 13. — P. 6365–6372.
37. Govekar R. B., Zingde S. M. Protein kinase C isoforms in human erythrocytes // Ann. Hematol. — 2001. — Vol. 80. — P. 531–534.
38. Houslay M. D., Kolch W. Cell-type specifi c integration of cross-talk between extracellular signal-regulated kinase and cAMP signaling // Mol. Pharm. — 2000. — Vol. 58, ¹ 4. — P. 659–668.
39. Clari G., Michielin E., Moret V. Interrelationships between protein kinases and spectrin phosphorylation in human erythrocytes // Biochim. Biophys. Acta. — 1981. — Vol. 8, ¹ 640 (1). — P. 240–251.
40. Erusalimsky J. D., Balas N., Milner Y. Possible identity of a membrane-bound with a soluble cyclic AMP-independent erythrocyte protein kinase that phosphorylates spectrin // Biochim. Biophys. Acta. — 1983. — Vol. 31, ¹ 756. — P. 171–181.
41. Eder P. S., Soong C. J., Tao M. Phosphorylation reduces the affi nity of protein 4.1 for Spectrin // Biochemistry. — 1986. — Vol. 8, ¹ 25 (7). — P. 1764–1770.
42. Horga J. F., Gisbert J., De Agustin J. C. A beta-2-adrenergic receptor activates adenilate cyclase in human erythrocyte membranes at physiological calcium plasma concentrations // Blood Cells Mol. Dis. — 2000. — Vol. 26, ¹ 3. — Ð. 223–228.
43. Sundquist J., Blas S. D., Hogan J. E. et al. The renergic receptor in human erythrocyte membranes mediates interaction in vitro of epinephrine and thyroid hormone at the membrane Ca2+ — ATPase // Cell. Signal. — 1992. — Vol. 4, ¹ 6. — P. 795–799.
44. Telen M. J. Erythrocyte adhesion receptors: blood group antigens and related molecules // Transfus. Med. Rev. — 2005. — Vol. 19, ¹ 1. — P. 32–44.
45. Tuvia S., Moses A., Gulayev N. et al. Beta-adrenergic agonists regulate cell membrane fl uctuations of human erythrocytes // J. Physiol. — 1999. — Vol. 516, ¹ 3. — P. 781–787.
46. Harrison M. L., Isaacson C. C., Burg D. L. et al. Phosphorylation of human erythrocyte band 3 by endogenous p72syk // J. Biol. Chem. — 1994. — Vol. 269, ¹ 2. — P. 955–959.
47. Kawakami M., Nagira T., Hayashi T. et al. Hypo-osmotic potentiation of acetylcholine-stimulated ciliary beat frequency through ATP release in rat tracheal ciliary cells // Exp. Physiol. — 2004. — Vol. 89, ¹ 6. — P. 739–751.
48. Tang L. C., Schoomaker E., Wiesmann W. P. Cholinergic agonists stimulate calcium uptake and cGMP formation in human erythrocytes // Biochim. Biophys. Acta. — 1984. — Vol. 772. — Ð. 235–238.
49. Olearczyk J. J., Stephenson A. H., Lonigro A. J., Sprague R. S. Heterotrimeric G protein Gi is involved in a signal transduction pathway for ATP release from erythrocytes // Am. J. Physiol. Heart Circ. Physiol. — 2004. — Vol. 286. — H940- H945.
50. Sprague R. S., Bowles E. A., Hanson M. S. et al. Prostacyclin analogs stimulate receptor-mediated cAMP synthesis and ATP release from rabbit and human erythrocytes // Microcirculation. — 2008. — Vol. 15, ¹ 5. — Ð. 461–471.
51. Olearczyk J. J., Stephenson A. H., Lonigro A. J., Sprague R. S. NO inhibits signal transduction pathway for ATP release from erythrocytes via its action on heterotrimeric G prote in Gi // Am. J. Physiol. Heart Circ. Physiol. — 2004. — Vol. 287. — H748-H754.
52. Willems C., Stel H. V. , van Aken W. G . , van Mourik J. A. Binding and inactivation of prostacyclin (PGI2) by human erythrocytes // Br. J. Haematol. — 1983. — Vol. 54, ¹ 1. — P. 43–52.
53. Gascard P., Cohen C. M. Absence of high-affi nity band 4.1 binding sites from membranes of glycophorin C- and D-defi cient (Leach phenotype) erythrocytes // Blood. — 1994. — Vol. 83, ¹ 4. — P. 1102–1108.
54. Cooper D. M., Brooker G. Ca2+-inhibited adenylate cyclase in cardiac tissue // Trends Pharmacol. Sci. — 1993. — Vol. 14. — P. 34–35.
55. Hilario S., Saldanha C., Martins-Silva J. The effect of adrenaline upon human erythrocyte properties. Sex-related diff erences? // Biorheology. — 1999. — Vol. 36, ¹ 1–2. — P. 124.
56. Hu D. E., Fan T. P. Suppression of VEGF induced angiogenesis by the protein tyrosine kinase inhibitor, lavendustin A // Br. J. Pharmacol. — 1995. — Vol. 114. — P. 262–269.
57. . Morris S. A., Bilezikian J. P. Evidence that forskolin activates turkey erythrocyte adenylate cyclase through a noncatalytic site // Arch. Biochem. Biophys. — 1983. — Vol. 220, ¹ 2. — P. 628–636.
58. Rasmussen H., Lake W., Alien J. E. The eff ect of catecholamines and prostaglandins upon human and rat erythrocytes // Biochim. Biophys. Acta. — 1975. — Vol. 411, ¹ 1. — P. 63–73.
59. Andrews D. A., Lu Y., Low Ph.S. Phorbol ester stimulates a protein kinase C-mediated agatoxin-TK-sensitive calcium permeability pathway in human red blood cells // Blood. — 2002. — Vol. 100, ¹ 9. — P. 3392–3399.
60. Takakuwa Y. Protein 4.1, a multifunctional protein of the erythrocyte membrane skeleton: structure and functions in erythrocytes and nonerythroid cells // Int. J. Hematol. — 2000. — Vol. 72, ¹ 3. — P. 298–309.
61. Sager G., Jacobsen S. Eff ect of plasma on human erythrocyte beta-adrenergic receptors // Biochem. Pharmacol. — 1985. — Vol. 34. — P. 3767–3771.
62. Muravyov A. V., Tikhomirova I. A., Maimistova A. A. et al. Crosstalk between adenylyl cyclase signaling pathway and Ca2+ regulatory mechanism under red blood cell microrheological changes // Clin. Hemorheol. Microcirc. — 2010. — Vol. 45, ¹ 2–4. — P. 337–345.
63. Rosen S. G., Berk M.A, Popp D. A. et al. Beta-2- and alpha- 2-adrenergic receptors and receptor coupling to adenylate cyclase in human mononuclear leukocytes and platelets in relation to physiological variations of sex steroids // J. Clin. Endocrinol. Metab. — 1984. — Vol. 58, ¹ 6. — P. 1068–1076.
64. Tepperman J., Tepperman H. Metabolic and endocrine physiology: an introductory text. — 5th ed. — Chicago- London: Year Book Medical Publishers, Inc, 1987. — 656 p.
65. Creighton J. R., Asada N., Cooper D. M., Steven T. Coordinate regulation of membrane cAMP by Ca 2 + -inhibited adenylyl cyclase and phosphodiesterase activities // Am. J. Physiol. Lung Cell Mol. Physiol. — 2003. — Vol. 284. — L100-L107.
66. Phillips P. G., Long L., Wilkins M. R., Morrell N. W. cAMP phosphodiesterase inhibitors potentiate eff ects of prostacyclin analogs in hypoxic pulmonary vascular remodeling // Am. J. Physiol. Lung Cell Mol. Physiol. — 2005. — Vol. 288. — L103-L115.
67. Ìóðàâüåâ À. Â., Ìàéìèñòîâà À. À., Òèõîìèðîâà È. À. è äð. Ðîëü ïðîòåèíêèíàç ìåìáðàíû ýðèòðîöèòîâ ÷åëî- âåêà â èçìåíåíèÿõ èõ äåôîðìèðóåìîñòè è àãðåãàöèè // Ôèçèîëîãèÿ ÷åëîâåêà. — 2012. — Ò. 38, ¹ 2. — Ñ. 94–100.
68. Laszlo R., Winkler C., W"ohrl S. et al. Infl uence of verapamil on tachycardia-induced alterations of PP1 and PP2A in rabbit atrium // Exp. Clin. Cardiol. — 2007. — Vol. 12, ¹ 4. — P. 175–178.
69. Êàðî Ê., Ïåäëè Ò., Øðîòåð Ð., Ñèä Ó. Ìåõàíèêà êðîâîîáðàùåíèÿ [Ïåð. ñ àíãë.]. — Ì.: Ìèð, 1981. — 623 ñ.
70. Secomb T. W. Flow-dependent rheological properties of blood in capillaries // Microvasc. Res. — 1987. — Vol. 34. — Ð. 46–58.
71. Kaul D. K., Fabry M. E. In vivo studies of sickle red blood cells // Microcirculation. — 2004. — Vol. 11. — P. 153–165.
72. Lipowsky H. H., Cram L. E., Justice W., Eppihimer M. J. Eff ect of erythrocyte deformability on in vivo red cell transit time and hematocrit and their correlation with in vitro fi lterability // Microvasc. Res. — 1993. — Vol. 46, ¹ 1. — P. 43–64.
73. Cokelet G. B., Meiselman H. J. Rheological comparison of hemoglobin solutions and erythrocyte suspensions // Science. — 1968. — Vol. 162. — P. 275–277.
74. Priers A. R., Secomb T. W. Rheology of the microcirculation // Clin. Hemorheol. Microcirc. — 2003. — Vol. 29, ¹ 3–4. — P. 143–148.
75. Secomb T. W., Pries A. R. Basic Principles of Hemodynamics // In: Handbook of Hemorheology and Hemodynamics. — Amsterdam: IOS Press, 2007. — Ð. 289–306.
76. Popel A. S., Johnson P. C. Microcirculation and hemorheology // Annu. Rev. Fluid Mech. — 2005. — Vol. 37. — Ð. 43–69.
77. Goldsmith H. L., Cokelet G. R., Gaehtgens P. Robin Fahraeus: evolution of his concepts in cardiovascular physiology // Am. J. Physiol. — 1989. — Vol. 257 (3 Pt 2). — H1005- H1015.
78. Pantely G. A., Swenson L. J., Tamblyn C. H. et al. Increased vascular resistance due to a reduction in red cell deformability in the isolated hind limb of swine // Microvasc. Res. — 1988. — Vol. 35. — P. 86–100.
79. Simchon S., Jan K. M., Chien S. Infl uence of reduced red cell deformability on regional blood fl ow // Am. J. Physiol. — 1987. — Vol. 253 (4 Pt 2). — H898-Í903.
80. Baskurt O. K., Sent"urk U. K., Dayan N. et al. Cyclosporine A aff ects red blood cell deformability in vivo but not in vitro in guinea pig // J. Pharmacol. Exp. Ther. — 1995. — Vol. 274. — P. 438–442.
81. Fischer D. J., Torrence N. J., Sprung R. J., Spence D. M. Determination of erythrocyte deformability and its correlation to cellular ATP release using micro bore tubing with diameters that approximate resistance vessels in vivo // Analyst. — 2003. — Vol. 128, ¹ 9. — P. 1163–1168.
82. Sprague R., Bowles E., Stumpf M. et al. Rabbit erythrocytes possess adenylyl cyclase type II that is activated by the heterotrimeric G proteins Gs and Gi // Pharmacol. Rep. — 2005. — Vol. 57 (Suppl) — P. 222–228.
83. Ellsworth M. L., Forrester T., Ellis C. G., Dietrich H. H. The erythrocyte as a regulator of vascular tone // Am. J. Physiol. Heart Circ. Physiol. — Vol. 269, ¹ 6. — P. 2155–2161.
84. Sprague R., Stephenson A., Bowles E. et al. Expression of the heterotrimeric G protein Gi and ATP release are impaired in erythrocytes of humans with diabetes mellitus // Adv. Exp. Med. Biol. — 2006. — Vol. 588. — P. 207–216.
85. Bozzo J., Hern M. R., Ordinas A. Reduced red cell deformability associated with blood fl ow and platelet activation: improved by dipyridamole alone or combined with aspirin // Cardiovasc. Res. — 1995. — Vol. 30 (Suppl 5). — P. 725–730.
86. Neu B., Sowemimo-Coker S.O., Meiselman H. J. Cell-cell affi nity of senescent human erythrocytes // Biophys. J. — 2003. — Vol. 85, ¹ 1. — Ð. 75–84.
87. Nash G. B. Red cell mechanics: what changes are needed to adversely aff ect in vivo circulation // Biorheology. — 1991. — Vol. 28. — P. 231–239.
88. Andreozzi G. M., Fava E., Barresi M. et al. Microcirculatory eff ects of the red cells aphaeresis in patients suff ering from peripheral arterial disease // Clin. Hemorheol. Microcirc. — 1995. — Vol. 15. — P. 406–409.
89. K"oksal C., Ercan M., Bozkurt A. K. Hemorheological variables in critical limb ischemia // Int. Angiol. — 2002. — Vol. 21, ¹ 4. — P. 355–359.
90. Wang X., Yang L., Liu Y. et al. Oxidized low-density lipoprotein (Ox-LDL) impacts on erythrocyte viscoelasticity and its molecular mechanism // J. Biomech. — 2009. — Vol. 42, ¹ 14. — P. 2394–2399.
91. Stoltz J. F. Red blood cell microrheology (clinical and pharmacological applications) // Ric. Clin. Lab. — 1983. — Vol. 13, Suppl. 3. — P. 53–70.
92. Cicco G., Cicco S. Hemorheological aspects in the microvasculature of several pathologies // Adv. Exp. Med. Biol. — 2007. — Vol. 599. — P. 7–15.
93. Ìóðàâüåâ À. Â., ßêóñåâè÷. Â.Â., Çàéöåâ Ë. Ã. è äð. Ãåìî- ðåîëîãè÷åñêèå ïðîôèëè ïàöèåíòîâ ñ àðòåðèàëüíîé ãè- ïåðòåíçèåé â ñî÷åòàíèè ñ ñèíäðîìîì ãèïåðâÿçêîñòè // Ôèçèîëîãèÿ ÷åëîâåêà. — 1998. — Ò. 24, ¹ 4. — Ñ. 113–117.
94. Ernst E., Matrai A. Blood rheology in athletes // J. Sports Med. and Phus. Fitness. — 1985. — Vol. 25, ¹ 4. — P. 207– 212.
95. Zannad F., Stoltz J. F. Blood rheology in arterial hypertension // J. Hypertens. 1992. — Vol. 10. — P. 69–78.
96. Vaya À., Martinez M., Labos M., Guiral I. The hemorheological profi le in off spring of hypertensive individuals // Clin. Hemorheol. — 1996. — Vol. 16, ¹ 3. — P. 235–243.
97. Cicco G., Pirrelli A. Red blood cell (RBC) deformability, RBC aggregability and tissue oxygenation in hypertension // Clin. Hemorheol. Microcirc. — 1999. — Vol. 21, ¹ 3–4. — P. 169–177.
98. Muravyov A. V., Cheporov S. V., Kislov N. V., Volkova E. L. Hemorheological changes in solid tumor patients after treatment with recombinant erythropoietin // Clin. Hemorheol. Microcirc. — 2009. — Vol. 41, ¹ 1. — P. 39–47.
99. Ìóðàâüåâ À. Â., ×åïîðîâ Ñ. Â. Ãåìàòîëîãè÷åñêèå è ãåìî- ðåîëîãè÷åñêèå àñïåêòû êîððåêöèè àíåìèé ïðåïàðàòà- ìè ýðèòðîïîýòèíà ó áîëüíûõ ñîëèäíûìè îïóõîëÿìè: ìîíîãðàôèÿ. — ßðîñëàâëü: Èçä-âî ßÃÏÓ èì. Ê. Ä. Óøèí- ñêîãî, 2009. — 162 ñ.
100. Muravyov A. V., Cheporov S. V., Kislov N. V. et al. Comparative effi ciency and hemorheological consequences of hemotransfusion and epoetin therapy in anemic cancer patients // Clin. Hemorheol. Microcirc. — 2010. — Vol. 44, ¹ 2. — P. 115–123.
101. Muravyov A. V., Tikhomirova I. A., Maimistova A. A. et al. Red blood cell aggregation changes are depended on its initial value: Eff ect of long-term drug treatment and shortterm cell incubation with drug // Clin. Hemorheol. Microcirc. — 2011. — Vol. 48, ¹ 4. — P. 231–240.
102. Shin S., Hou J. X., Suh J. S., Singh M. Validation and application of a microfl uidic ektacytometer (RheoScan-D) in measuring erythrocyte deformability // Clin. Hemorheol. Microcirc. — 2007. — Vol. 37. — Ð. 319–328.
103. Muravyov A. V. Yakusevich V. V., Maimistova A. A. et al. Hemorheological effi ciency of drugs, targeting on intracellular phosphodiesterase activity: in vitro study // Clin. Hemorheol. Microcirc. — 2007. — Vol. 36, ¹ 4. — P. 327–334.
104. Sabo A., Jakovljevi Stanuloviet al. Red blood cell deformability in diabetes mellitus: eff ect of phytomenadione // Int. J. Clin. Pharmacol. Ther. Toxicol. — 1993. — Vol. 31, ¹ 1. — P. 1–5.
105. Forst T., Kunt T. Eff ects of C-peptide on microvascular blood flow and blood hemorheology // Exp. Diabesity Res. — 2004. — Vol. 5, ¹ 1. — P. 51–64.
106. Hach T., Forst T., Kunt T. et al. C-peptide and its C-terminal fragments improve erythrocyte deformability in type 1 diabetes patients // Exp. Diabetes Res. — 2008. — Vol. 45. — P. 730–736.
107. Schut N. H., van Arkel E. C., Hardeman M. R. et al. Blood and plasma viscosity in diabetes: possible contribution to late organ complications? // Diabetes Res. — 1992. — Vol. 19, ¹ 1. — P. 31–35.
108. Vi J., M Z., Krky G. et al. Hemorheologic factors in hypertensive and diabetic retinopathy // Orv. Hetil. — 2001. — Vol. 20, ¹ 142 (20). — P. 1045–1048.
109. Negrean V., Suciu I., S^ampelean D., Cozma A. Rheological changes in diabetic microangiopathy // Rom. J. Intern. Med. — 2004. — Vol. 42, ¹ 2. — P. 407–413.
110. Sauvage M., Mazi`ere P., Fathallah H., Giraud F. Insulin stimulates NHE1 activity by sequential activation of phosphatidylinositol 3-kinase and protein kinase C-zeta in human erythrocytes // Eur. J. Biochem. — 2000. — Vol. 267, ¹ 4. — P. 955–962.
111. Ceolotto G., Sartori M., Felice M. et al. Eff ect of protein kinase C and insulin on Na+/H+ exchange in red blood cells of essential hypertensives // J. Hum. Hypertens. — 1999. — Vol. 13, ¹ 5. — P. 321–327.
112. Oliveira S., Seok S. C. A matrix-based multilevel approach to identify functional protein modules // Int. J. Bioinform. Res. Appl. — 2008. — Vol. 4, ¹ 1. — P. 11–27.
113. Semplicini A., Ceolotto G., Felice M. et al. Posttranslational eff ects of protein kinase C and insulin on red cell membrane phosphorylation and cation heteroexchange in hypertension // Blood Press Suppl. — 1996. — Vol. 1. — P. 55–58.
114. Ling E., Danilov Y. N., Cohen C. M. Modulation of red cell band 4.1 function by cAMP-dependent kinase and protein kinase C phosphorylation // J. Biol. Chem. — 1988. — Vol. 15, ¹ 263. — P. 2209–2216.
115. Muravyov A. V., Meiselman J. H., Yakusevich V. V., Zamishlayev A. V. Eff ects of antihypertensive therapy on hemorheological profi les in female hypertensive patients with initially low or high whole blood viscosity // Clin. Hemorheol. Microcirc. — 2002. — Vol. 26, ¹ 2. — P. 125–135.
116. Starzyk D., Korbut R., Gryglewski R. J. Eff ects of nitric oxide and prostacyclin on deformability and aggregability of red blood cells of rats ex vivo and in vitro // J. Physiol. Pharmacol. — 1999. — Vol. 50. — Ð. 629–637.