Glucose Reduces the Osmopressor Response in Connection with the Tyrosine Phosphorylation of Focal Adhesion Kinase in Red Blood Cells

10.4103/CJP.CJP_32_20

You-Hsiang Chu；Ying-Hsuan Tai；Chun-Chang Yeh；Mei-Yung Tsou；Herng-Sheng Lee；Shung-Tai Ho；Min-Hui Li；Tso-Chou Lin；Chih-Cherng Lu

Focal adhesion kinase ； glucose ； osmopressor ； red blood cells

The Chinese Journal of Physiology

63卷3期（2020 / 06 / 30）

128 - 136

英文

Glucose ingestion attenuates the water ingestion-induced increase in the total peripheral vascular resistance and orthostatic tolerance. We investigated the gastrointestinal physiology of glucose by examining the effect of glucose ingestion on the functional expression of focal adhesion kinase (FAK) in red blood cell (RBC) membrane. This study was performed in 24 young, healthy subjects. Blood samples were collected at 5 min before and 25 min and 50 min after an ingestion of 10% glucose water 500 mL, water 500 mL, or normal saline 500 mL. We determined glucose and osmolality in plasma, and phosphorylation of aquaporin 1 (AQP1), glucose transporter 1 (Glut1), and FAK in RBC membrane. Our results showed that glucose ingestion reduced the rise of peripheral vascular resistance after water ingestion and upregulated the serine phosphorylation of Glut1. It also lowered both the serine phosphorylation of FAK and tyrosine phosphorylation of AQP1, compared with the ingestion of either water or saline. In an ex vivo experiment, glucose activated the Glut1 receptor and subsequently reduced the expression of FAK compared with 0.8% saline alone. We concluded that glucose activates Glut1 and subsequently lowers the functional expression of FAK, a cytoskeleton protein of RBCs. The functional change in the RBC membrane proteins in connection with the attenuation of osmopressor response may elucidate the pathophysiology of glucose in postprandial hypotension.

1. Tsai, SH,Lin, JY,Lin, YC,Liu, YP,Tung, CS(2020).Portal vein innervation underlying the pressor effect of water ingestion with and without cold stress.Chin J Physiol,63,53-59.
   連結：
2. Arold, ST,Hoellerer, MK,Noble, ME(2002).The structural basis of localization and signaling by the focal adhesion targeting domain.Structure,10,319-327.
3. Aronow, WS,Ahn, C(1997).Association of postprandial hypotension with incidence of falls, syncope, coronary events, stroke, and total mortality at 29-month follow-up in 499 older nursing home residents.J Am Geriatr Soc,45,1051-1053.
4. Bianchi, J,Rose, RC(1986).Glucose-independent transport of dehydroascorbic acid in human erythrocytes.Proc Soc Exp Biol Med,181,333-337.
5. Buys, AV,van Rooy, MJ,Soma, P,van Papendorp, D,Lipinski, B,Pretorius, E(2013).Changes in red blood cell membrane structure in type 2 diabetes: A scanning electron and atomic force microscopy study.Cardiovasc Diabetol,12,25.
6. Cho, YI,Mooney, MP,Cho, DJ(2008).Hemorheological disorders in diabetes mellitus.J Diabetes Sci Technol,2,1130-1138.
7. Chu, YH,Hsu, YJ,Lee, HS,Ho, ST,Tung, CS,Tseng, CJ(2013).The osmopressor response is linked to upregulation of aquaporin-1 tyrosine phosphorylation on red blood cell membranes.Hypertension,62,197-202.
8. Diez-Silva, M,Dao, M,Han, J,Lim, CT,Suresh, S(2010).Shape and biomechanical characteristics of human red blood cells in health and disease.MRS Bull,35,382-388.
9. Dinkla, S,Wessels, K,Verdurmen, WP,Tomelleri, C,Cluitmans, JC,Fransen, J(2012).Functional consequences of sphingomyelinase-induced changes in erythrocyte membrane structure.Cell Death Dis,3,e410.
10. Guelen, I,Westerhof, BE,van der Sar, GL,Van Montfrans, GA,Kiemeneij, F,Wesseling, KH(2003).Finometer, finger pressure measurements with the possibility to reconstruct brachial pressure.Blood Press Monit,8,27-30.
11. Helgerson, AL,Carruthers, A(1987).Equilibrium ligand binding to the human erythrocyte sugar transporter. Evidence for two sugar-binding sites per carrier.J Biol Chem,262,5464-5475.
12. Hirayama, M,Watanabe, H,Koike, Y,Hasegawa, Y,Kanaoke, Y,Sakurai, N(1993).Postprandial hypotension: Hemodynamic differences between multiple system atrophy and peripheral autonomic neuropathy.J Auton Nerv Syst,43,1-6.
13. Jones, KL,MacIntosh, C,Su, YC,Wells, F,Chapman, IM,Tonkin, A(2001).Guar gum reduces postprandial hypotension in older people.J Am Geriatr Soc,49,162-167.
14. Jordan, J,Shannon, JR,Black, BK,Ali, Y,Farley, M,Costa, F(2000).The pressor response to water drinking in humans: A sympathetic reflex?.Circulation,101,504-509.
15. Khalili, AA,Ahmad, MR(2015).A review of cell adhesion studies for biomedical and biological applications.Int J Mol Sci,16,18149-18184.
16. Lee, EE,Ma, J,Sacharidou, A,Mi, W,Salato, VK,Nguyen, N(2015).A protein kinase C phosphorylation motif in GLUT1 affects glucose transport and is mutated in GLUT1 deficiency syndrome.Mol Cell,58,845-853.
17. Li, S,Kim, M,Hu, YL,Jalali, S,Schlaepfer, DD,Hunter, T(1997).Fluid shear stress activation of focal adhesion kinase. Linking to mitogen-activated protein kinases.J Biol Chem,272,30455-30462.
18. Lu, CC,Diedrich, A,Tung, CS,Paranjape, SY,Harris, PA,Byrne, DW(2003).Water ingestion as prophylaxis against syncope.Circulation,108,2660-2665.
19. Lu, CC,Li, MH,Ho, ST,Lu, CL,Lin, JC,Lin, TC(2008).Glucose reduces the effect of water to promote orthostatic tolerance.Am J Hypertens,21,1177-1182.
20. Lu, CC,Li, MH,Lin, TC,Chen, TL,Chen, RM,Tung, CS(2012).Water ingestion reduces skin blood flow through sympathetic vasoconstriction.Clin Auton Res,22,63-69.
21. Lu, D,Kassab, GS(2011).Role of shear stress and stretch in vascular mechanobiology.J R Soc Interface,8,1379-1385.
22. Madonna, R,Geng, YJ,Shelat, H,Ferdinandy, P,de Caterina, R(2014).High glucose-induced hyperosmolarity impacts proliferation, cytoskeleton remodeling and migration of human induced pluripotent stem cells via aquaporin-1.Biochim Biophys Acta,1842,2266-2275.
23. Malik, VS,Popkin, BM,Bray, GA,Després, JP,Hu, FB(2010).Sugar-sweetened beverages, obesity, type 2 diabetes mellitus, and cardiovascular disease risk.Circulation,121,1356-1364.
24. Malik, VS,Schulze, MB,Hu, FB(2006).Intake of sugar-sweetened beverages and weight gain: A systematic review.Am J Clin Nutr,84,274-288.
25. Mathias, CJ,da Costa, DF,Fosbraey, P,Bannister, R,Wood, SM,Bloom, SR(1989).Cardiovascular, biochemical and hormonal changes during food-induced hypotension in chronic autonomic failure.J Neurol Sci,94,255-269.
26. Mitra, SK,Hanson, DA,Schlaepfer, DD(2005).Focal adhesion kinase: In command and control of cell motility.Nat Rev Mol Cell Biol,6,56-68.
27. Montel-Hagen, A,Kinet, S,Manel, N,Mongellaz, C,Prohaska, R,Battini, JL(2008).Erythrocyte Glut1 triggers dehydroascorbic acid uptake in mammals unable to synthesize vitamin C.Cell,132,1039-1048.
28. Morley, JE(2001).Editorial: Postprandial hypotension-The ultimate Big Mac attack.J Gerontol A Biol Sci Med Sci,56,M741-M743.
29. O’Donovan, D,Feinle, C,Tonkin, A,Horowitz, M,Jones, KL(2002).Postprandial hypotension in response to duodenal glucose delivery in healthy older subjects.J Physiol,540,673-679.
30. Owen, JD,Ruest, PJ,Fry, DW,Hanks, SK(1999).Induced focal adhesion kinase (FAK) expression in FAK-null cells enhances cell spreading and migration requiring both auto- and activation loop phosphorylation sites and inhibits adhesion-dependent tyrosine phosphorylation of Pyk2.Mol Cell Biol,19,4806-4818.
31. Pelikánová, T,Kohout, M,Válek, J,Base, J,Stefka, Z(1991).Fatty acid composition of serum lipids and erythrocyte membranes in type 2 (non-insulin-dependent) diabetic men.Metabolism,40,175-180.
32. Potter, JF,Heseltine, D,Hartley, G,Matthews, J,MacDonald, IA,James, OF(1989).Effects of meal composition on the postprandial blood pressure, catecholamine and insulin changes in elderly subjects.Clin Sci,77,265-272.
33. Raj, SR,Coffin, ST(2013).Medical therapy and physical maneuvers in the treatment of the vasovagal syncope and orthostatic hypotension.Prog Cardiovasc Dis,55,425-433.
34. Rathmell, JC,Vander Heiden, MG,Harris, MH,Frauwirth, KA,Thompson, CB(2000).In the absence of extrinsic signals, nutrient utilization by lymphocytes is insufficient to maintain either cell size or viability.Mol Cell,6,683-692.
35. Schroeder, C,Bush, VE,Norcliffe, LJ,Luft, FC,Tank, J,Jordan, J(2002).Water drinking acutely improves orthostatic tolerance in healthy subjects.Circulation,106,2806-2811.
36. Schwartz, RS,Madsen, JW,Rybicki, AC,Nagel, RL(1991).Oxidation of spectrin and deformability defects in diabetic erythrocytes.Diabetes,40,701-708.
37. Scott, EM,Greenwood, JP,Stoker, JB,Gilbey, SG,Mary, DA(2000).Water drinking and sympathetic activation.Lancet,356,2013.
38. Shannon, JR,Diedrich, A,Biaggioni, I,Tank, J,Robertson, RM,Robertson, D(2002).Water drinking as a treatment for orthostatic syndromes.Am J Med,112,355-360.
39. Tai, YH,Chu, YH,Wu, HL,Lin, SM,Tsou, MY,Huang, CH(2020).High-dose nitroglycerin administered during rewarming preserves erythrocyte deformability in cardiac surgery with cardiopulmonary bypass.Microcirculation,27,e12608.
40. Wu, JC,Chen, YC,Kuo, CT,Wenshin, Yu, H,Chen, YQ,Chiou, A(2015).Focal adhesion kinase-dependent focal adhesion recruitment of SH2 domains directs SRC into focal adhesions to regulate cell adhesion and migration.Sci Rep,5,18476.
41. Yamamoto, H,Lee, CE,Marcus, JN,Williams, TD,Overton, JM,Lopez, ME(2002).Glucagon-like peptide-1 receptor stimulation increases blood pressure and heart rate and activates autonomic regulatory neurons.J Clin Invest,110,43-52.
42. Zhao, H,Sun, J,Shao, J,Zou, Z,Qiu, X,Wang, E(2019).Glucose transporter 1 promotes the malignant phenotype of non-small cell lung cancer through integrin β1/Src/FAK signaling.J Cancer,10,4989-4997.