G protein-linked cell signaling and cardiovascular functions in diabetes/hyperglycemia

Cell Biochemistry and Biophysics

Volumn 44, Issue 1, 2006, Pages 51-64

  Hashim, Shehla ^a   Li, Yuan ^a   Anand Srivastava, Madhu B ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Cardiovascular function; Diabetes; G protein linked cell signaling; Hyperglycemia

Indexed keywords

EID: 30744460377     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1385/cbb:44:1:051     Document Type: Review

References (109)

1. Kessler, I. I. (1971) Mortality experience of diabetic patients. A twenty-six-year follow-up study. Am. J. Med. 51, 715-724.
2. Kannel, W. B. and McGee, D. L. (1979) Diabetes and glucose tolerance as risk factors for cardiovascular disease: the Framingham study. Diabetes Care 2, 120-126.
3. Gilman, A. G. (1984) G proteins and dual control of adenylate cyclase. Cell 36, 577-579.
4. Stryer, L. and Bourne, H. R. (1986) G proteins: a family of signal transducers. Annu. Rev. Cell Biol. 2, 391-419.
5. Spiegel, A. M. (1987) Signal transduction by guanine nucleotide binding proteins. Mol. Cell Endocrinol. 49, 1-16.
6. Murakami, T. and Yasuda, H. (1986) Rat heart cell membranes contain three substrates for cholera toxin-catalyzed ADP-ribosylation and a single substrate for pertussis toxin-catalyzed ADP-ribosylation. Biochem. Biophys. Res. Commun. 138, 1355-1361.
7. Robishaw, J. D., Smigel, M. D., and Gilman, A. G. (1986) Molecular basis for two forms of the G protein that stimulates adenylate cyclase. J. Biol. Chem. 261, 9587-9590.
8. Bray, P, Carter, A., Simons, C., Guo, V., et al. (1986) Human cDNA clones for four species of Gαs signal transduction protein. Proc. Natl. Acad. Sci. USA 83, 8893-8897.
9. Itoh, H., Kozasa, T., Nagata, S., et al. (1986) Molecular cloning and sequence determination of cDNAs for α subunits of the guanine nucleotide-binding proteins Gs, Gi, and Go from rat brain. Proc. Natl. Acad. Sci. USA 83, 3776-3780.
10. Jones, D. T., and Reed, R. R. (1987) Molecular cloning of five GTP-binding protein cDNA species from rat olfactory neuroepithelium. J. Biol. Chem. 262, 14241-14249.
11. Itoh, H., Toyama, R., Kozasa, T., et al. (1988) Presence of three distinct molecular species of Gi protein: a subunit structure of rat cDNA and human genomic DNAs. J. Biol. Chem. 263, 6656-6664.
12. Wong, Y. H., Conklin, B. R., and Bourne, H. R. (1992) Gz-mediated hormonal inhibition of cyclic AMP accumulation. Science 255, 339-342
13. Brown, A. M. and Birnbaumer, L. (1988) Direct G protein gating of ion channels. Am. J. Physiol. 254, H401-H410.
14. Simon, M. I., Strathmann, M. P., and Gautam, N. (1991) Diversity of G proteins in signal transduction. Science 252, 802-808.
15. Cali, J. J., Balcueva, E. A., Rybalkin, I., and Robishaw, J. D. (1992) Selective tissue distribution of protein γ subunits, including a new form of the γ subunits identified by cDNA cloning. J. Biol Chem. 267, 24,023-24,027.
16. Tang, W. J. and Gilman, A. G. (1991) Type-specific regulation of adenylyl cyclase by G protein βγ subunits. Science 254, 1500-1503.
17. Wickman, K. D., Iniguez-Lluhl, J. A., Davenport, P. A., et al. (1994) Recombinant G-protein βγ-subunits activate the muscarinic-gated atrial potassium channel. Nature 368, 255-257.
18. Ishikawa, Y. and Homcy, C. J. (1997) The adenylyl cyclases as integrators of transmembrane signal transduction. Circ. Res. 80, 297-304.
19. Katsushika, S., Chen, L., Kawabe, J., et al. (1992) Cloning and characterization of a sixth adenylyl cyclase isoform: types V and VI constitute a subgroup within the mammalian adenylyl cyclase family. Proc. Natl. Acad. Sci. USA. 89, 8774-8778
20. Premont, R. T., Chen, J., Ma, H. W., Ponnapalli, M., and Iyengar, R. (1992) Two members of a widely expressed subfamily of hormone-stimulated adenylyl cyclases. Proc. Natl. Acad. Sci. USA 89, 9809-9813.
21. Toro, M. J., Montoya, E., and Birnbaumer, L. (1987) Inhibitory regulation of adenylyl cyclases. Evidence inconsistent with βγ-complexes of Gi proteins mediating hormonal effects by interfering with activation of Gs. Mol. Endocrinol. 10, 669-676.
22. Taussig, R., Quarmby, L. M., and Gilman, A. G. (1993) Regulation of purified type I and type II adenylylcyclases by G protein βγsubunits. J. Biol. Chem. 268, 9-12.
23. Cassel, D. and Pfeuffer, T. (1978) Mechanism of cholera toxin action: covalent modification of the guanyl nucleotide-binding protein of the adenylate cyclase system. Proc. Natl. Acad. Sci. USA. 75, 2669-2673.
24. Hewlett, E. L., Cronin, M. J., Moss, J., Anderson, H., Myers, G. A., and Pearson, R. D. (1984) Pertussis toxin: lessons from biological and biochemical effects in different cells. Adv. Cyclic Nucleotide Protein Phosphorylation Res. 17, 173-182.
25. Ui, M. (1984) Islet-activating protein, pertussis toxin: a probe for function of the inhibitory guanine nucleotide regulatory component of adenylate cyclase. Trends Pharmacol. Sci. 5, 277-279.
26. Katada, T., and Ui, M. (1982) DP ribosylation of the specific membrane protein of C6 cells by islet-activating protein associated with modification of adenylate cyclase activity. J. Biol. Chem. 257, 7210-7216.
27. Hazeki, O. and Ui, M. (1981) Modification by islet-activating protein of receptor-mediated regulation of cyclic cAMP accumulation in isolated rat heart cells. J Biol Chem. 256, 2856-2862.
28. Hsu, W. H., Rudolph, U., Sanford, J., et al. (1990) Molecular cloning of a novel splice variant of the α subunit of the mammalian Go protein. J. Biol. Chem. 265, 11,220-11,226.
29. Strathmann, M., Wilkie, T. M., and Simon, M. I. (1990) Alternative splicing produces transcripts encoding two forms of the α subunit of GTP-binding protein Go. Proc. Natl. Acad. Sci. USA 87, 6477-6481.
30. Moriarty, T. M., Padrell, E., Carty, D. J., Omri, G., Landau, E. M., and Iyengar R. (1990) Go protein as signal transducer in the pertussis toxin-sensitive phosphatidylinositol pathway. Nature 343, 79-82.
31. 2+ channels in sensory neurons. Proc. Natl. Acad. Sci. USA 85, 3633-3637.
32. Kleuss, C., Scherubl, H., Hescheler, J., Schultz, G., and Wittig, B. (1992) Different β-subunits determine G-protein interaction with transmembrane receptors. Nature 358, 424-426.
33. Strittmatter, S. M., Valenzuela, D., Kennedy, T. E., Neer, E. J., and Fishman, M. C. (1990) G0 is a major growth cone protein subject to regulation by GAP-43. Nature 344, 836-841.
34. Katada, J., Imuna, M., and Ui, M. (1986) Two guanine nucleotide-binding proteins in rat brain serving as the specific substrate of islet-activating protein, pertussis toxin. Interaction of the α-subunits with β subunits in development of their biological activities. J. Biol. Chem. 261, 8182-8191.
35. Pang, I. H. and Sternweis, P. C. (1990) Purification of unique α subunits of GTP-binding regulatory proteins (G proteins) by affinity chromatography with immobilized βγ subunits. J. Biol. Chem. 265, 18,707-18,712.
36. Simon, M. I., Strathmann, M. P., and Gautam, N. (1991) Diversity of G proteins in signal transduction. Science 252, 802-808.
37. Kim, D., Lewis, D. L., Graziadei, L., Neer, E. J., Bar-Sagi, D., and Clapham, D. E. (1989) G-protein βγ-subunits activate the cardiac muscarinic K+-channel via phospholipase A2. Nature 337, 557-560.
38. Park, D., John, D. Y., Kriz, R., Knopf, J., and Rhee, S. G. (1992) Cloning, sequencing, expression, and Gq-independent activation of phospholipase C-β 2. J. Biol. Chem. 267, 16,048-16,055.
39. Inoguchi, T., Battan, R., Handler, E., Sportsman, J. R., Heath, W., and King, G. L. (1992) Preferential elevation of protein kinase C isoform βII and diacylglycerol levels in the aorta and heart of diabetic rats: differential reversibility to glycemic control by islet cell transplantation. Proc. Natl. Acad. Sci. USA. 89, 11,059-11,063.
40. Craven, P. A. and DeRubertis, F. R. (1989) Protein kinase C is activated in glomeruli from streptozotocin diabetic rats. Possible mediation by glucose. J. Clin. Invesitg. 83, 1667-1675.
41. Koya, D. and King, G. L. (1998) Protein kinase C activation and the development of diabetic complications. Diabetes 47, 859-866.
42. Weber, L. P. and Macleod, K. M. (1997) Influence of streptozotocin diabetes on the α-1 adrenoceptor and associated G proteins in rat arteries. J. Pharmacol. Exp. Ther. 283, 1469-1478.
43. 2 but not noradrenaline, of aortae from rats with streptozotocin-induced mellitus. Br. J. Pharmacol. 104, 928-932.
44. Turlapaty, P. D., Lum, G., and Altura, B. M. (1980) Vascular responsiveness and serum biochemical parameters in alloxan diabetes mellitus. Am. J. Physiol. 239, E412-E421.
45. Ballermann, B. J., Skorecki, K. L., and Brenner, B. M. (1984) Reduced glomerular angiotensin II receptor density in early untreated diabetes mellitus in the rat. Am. J. Physiol. 247, F110-F116.
46. Wilkes, B. M. (1987) Reduced glomerular angiotensin II receptor density in diabetes mellitus in the rat: time curse and mechanism. Endocrinology 120, 1291-1298.
47. Abebe, W. and MacLeod, K. M. (1990) Protein kinase C-mediated contractile responses of arteries from diabetic rats. Br. J. Pharmacol. 101, 465-471
48. Abebe, W. and MacLeod, K. M. (1991) Influence of diabetes on norepinephrine-induced inositol 1,4,5-trisphosphate levels in rat aorta. Life Sci. 49, PL85-PL90.
49. Wang, R., Wu, Y., Tang, G., Wu, L., and Hanna, S. T. (2000) Altered L-type Ca(2+) channel currents in vascular smooth muscle cells from experimental diabetic rats. Am. J. Physiol. 278, H714-H722
50. Park, S. H., Choi, H. J., Lee, J. H, Yang, I. S., and Han, H. J. (2001) High glucose stimulates Ca2+ uptake via cAMP and PLC/PKC pathways in primary cultured renal proximal tubule cells. Kidney Blood Press Res. 24, 10-17.
51. Hargrove, G. M., Dufresne, J., Whiteside, C., Muruve, D. A., and Wong, N. C. (2000) Diabetes mellitus increases endothelin-1 gene transcription in rat kidney. Kidney Int. 58, 1534-1545.
52. Park, J. Y., Takahara, N., Gabriele, A., et al. (2000) Induction of endothelin-1 expression by glucose: an effect of protein kinase C activation. Diabetes 49, 1239-1248.
53. Makino, A. and Kamata, K. (2000) Time-course changes in plasma endothelin-1 and its effects on the mesenteric arterial bed in streptozotocin-induced diabetic rats. Diabetes Obes Metab. 2, 47-55.
54. Balsiger, B., Rickenbacher, A., Boden, P. J., et al. (2002) Endothelin A-receptor blockade in experimental diabetes improves glucose balance and gastrointestinal function. Clin. Sci. 103 (Suppl 48), 430S-433S.
55. McKenna, K., Smith, D., Tormey, W., and Thompson, C .J. (2000) Acute hyperglycaemia causes elevation in plasma atrial natriuretic peptide concentrations in type 1 diabetes mellitus. Diabetes Med. 17, 512-517.
56. Shin, S. J., Lee, Y. J., Tan, M. S., Hsieh, T. J., and Tsai J. H. (1997) Increased atrial natriuretic peptide mRNA expression in the kidney of diabetic rats. Kidney Int. 51, 1100-1105.
57. Kook, H., Lee, J., Kim, S. W., Kim, S. W., and Baik, Y. H. (2002) Augmented natriuretic peptide-induced guanylyl cyclase activity and vasodilation in experimental hyperglycemic rats. Jpn. J. Pharmacol. 88, 167-173.
58. Natarajan, R., Bai, W., Lanting, L., Gonzales, N., and Nadler, J. E. (1997) Effects of high glucose on vascular endothelial growth factor expression in vascular smooth muscle cells. Am. J. Physiol. 273, H2224-H2231.
59. Hayashi, S., Morishita, R., Matsushita, H., et al. (2000) Cyclic AMP inhibited proliferation of human aortic vascular smooth muscle cells, accompanied by induction of p53 and p21. Hypertension 35, 237-243.
60. Dubey, R. K., Gillespie, D. G., Mi, Z., et al. (2000) Estradiol inhibits smooth muscle cell growth in part by activating the cAMP-adenosine pathway. Hypertension 35, 262-266.
61. Gamet, L., Murat, J. C., Remaury, A., et al. (1992) Vasoactive intestinal peptide and forskolin regulate proliferation of the HT29 human colon adenocarcinoma cell line. J. Cell Physiol. 150, 501-509.
62. Rojas, S., Rojas, R., Lamperti, L., Casanello, P., and Sobrevia, L. (2003) Hyperglycaemia inhibits thymidine incorporation and cell growth via protein kinase C, mitogen-activated protein kinases and nitric oxide in human umbilical vein endothelium. Exp. Physiol. 88, 209-219.
63. Schmidt, C. M., McKillop, I. H., Cahill, P. A., and Sitzmann, J. V. (1999) The role of cAMP-MAPK signalling in the regulation of human hepatocellular carcinoma growth in vitro. Eur. J. Gastroenterol. Hepatol. 11, 1393-1399.
64. Amano, H., Haysahi, I., Yoshida, S., Yoshimura, H., and Majima, M. (2002) Cyclooxygenase-2 and adenylate cyclase/protein kinase A signaling pathway enhances angiogenesis through induction of vascular endothelial growth factor in rat sponge implants. Hum. Cell 15, 13-24.
65. Amano, H., Ando, K., Minamida, S., et al. (2001) Adenylate cyclase/protein kinase A signaling pathway enhances angiogenesis through induction of vascular endothelial growth factor in vivo. Jpn. J. Pharmacol. 87, 181-188.
66. Yasunari, K., Kohno, M., Kano, H., Yokokawa, K., Minami, M., and Yoshikawa, J. (1999) Antioxidants improve impaired insulin-mediated glucose uptake and prevent migration and proliferation of cultured rabbit coronary smooth muscle cells induced by high glucose. Circulation 99, 1370-1378.
67. Fujita, N., Furukawa, Y., Du, J., et al. (2002) Hyperglycemia enhances VSMC proliferation with NF-κB activation by angiotensin II and E2F-1 augmentation by growth factors. Mol. Cell. Endocrinol. 192, 75-84.
68. Yasumari, K., Kohmo, M., Kano, H., Yokokawa, K., Minami, M., and Yoshikawa, J. (1999) Antioxidants improve insulin-mediated glucose uptake and prevent migration and proliferation of cultured rabbit coronary smooth muscle cells induced by high glucose. Circulation 99, 1370-1378.
69. Giugliano, D., Marfella, R., Coppola, L., et al. (1997) Vascular effects of acute hyperglycemia in humans are reversed by L-arginine. Evidence for reduced availability of nitric oxide during hyperglycemia. Circulation 95, 1783-1790.
70. Lash, J. M., Nase, G. P., and Bohlen, H. G. (1999) Acute hyperglycemia depresses arteriolar NO formation in skeletal muscle. Am. J. Physiol. 277, H1513-H1520.
71. Gade, P. V., Andrades, J. A., Nimni, et al. (1997) Nitric oxide mediates hyperglycemia-induced defective migration in cultured endothelial cells. J. Vasc. Surg. 26, 319-326.
72. Kihara, M. and Low, P. A. (1995) Impaired vasoreactivity to nitric oxide in experimental diabetic neuropathy. Exp. Neurol. 132, 180-185.
73. Cosentino, F., Hishikawa, K., Katusic, Z. S., and Luscher, T. F. (1997) High glucose increases nitric oxide synthase expression and superoxide anion generation in human aortic endothelial cells. Circulation 96, 25-28.
74. Feldman, A. M., Cates, A. E., Veazey, W. B., et al. (1988) Increase of the 40,000-mol wt pertussis toxin substrate (G protein) in the failing human heart. J. Clin. Investig. 82, 189-197
75. Anand-Srivastava, M. B. (1992) Enhanced expression of inhibitory guanine nucleotide regulatory protein in spontaneously hypertensive rats. Relationship to adenylate cyclase inhibition. Biochem. J. 288, 79-85.
76. Thibault, C. and Anand-Srivastava, M. B. (1992) Altered expression of G-protein mRNA in spontaneously hypertensive rats. FEBS Lett. 313, 160-164.
77. Lynch, C. J., Blackmore, P. F., Johnson, E. H., Wange, R. L., Krone, P. K., and Exton, J. H. (1989) Guanine nucleotide binding regulatory proteins and adenylate cyclase in livers of streptozotocin- and BB/Wor-diabetic rats. Immunodetection of Gs and Gi with antisera prepared against synthetic peptides. J. Clin. Investig. 83, 2050-2062.
78. Bushfield, M., Griffiths, S. L., Murphy, G. J., et al. (1990) Diabetes-induced alterations in the expression, functioning and phosphorylation state of the inhibitory guanine nucleotide regulatory protein Gi-2 in hepatocytes. Biochem. J. 271, 365-372.
79. Caro, J. F., Raju, M. S., Caro, et al. (1994) Guanine nucleotide binding regulatory proteins in liver from obese humans with and without type II diabetes: evidence for altered "cross-talk" between the insulin receptor and Gi-proteins. J. Cell Biochem. 54, 309-319.
80. Strassheim, D., Palmer, T., and Houslay, M. D. (1991) Genetically acquired diabetes: adipocyte guanine nucleotide regulatory protein expression and adenylate cyclase regulation. Biochim. Biophys. Acta 1096, 121-126.
81. Livingstone, C., McLellan, A. R., McGregor, M. A., et al. (1991) Altered G-protein expression and adenylate cyclase activity in platelets of non-insulin-dependent diabetic (NIDDM) male subjects. Biochim. Biophys. Acta 1096, 127-133.
82. Hadjiconstantinou, M., Qu, Z. X., Moroi-Fetters, S. E., and Neff, N. H. (1988) Apparent loss of Gi protein activity in the diabetic retina. Eur. J. Pharmacol. 149, 193-194.
83. Hattori, Y., Matsuda, N., Sato, A., et al. (2000) Predominant contribution of the G protein-mediated mechanism to NaF-induced vascular contractions in diabetic rats: association with an increased level of G(qα) expression. J. Pharmacol. Exp. Ther. 292, 761-768.
84. Zheng, X. L., Guo, J., Wang, H., and Malbon, C. C. (1998) Expression of constitutively activated Giα2 in vivo ameliorates streptozotocin-induced diabetes. J. Biol. Chem. 273, 23,649-23,651.
85. Moxham, C. M. and Malbon, C. C. (1996) Insulin action impaired by deficiency of the G-protein subunit Gi α. Nature 379, 840-844.
86. Griffiths, S. L., Knowler, J. J., and Housley, M. D. (1990) Diabetes-induced changes in guanine nucleotide regulatory protein mRNA detected using synthetic oligonucleotie probes. Eur. J. Biochem. 193, 367-374.
87. Hashim, S., Liu, Y. Y., Wang, R., and Anand-Srivastava, M. B. (2002) Streptozotocin-induced diabetes impairs G-protein linked signal transduction I vascular smooth muscle. Mol. Cell Biochem. 240, 57-65.
88. Phan, H. H., Boissard, C., Pessah, M., et al. (2000) Decreased ADP-ribosylation of the Giα (olf) and Gα(s) subunits by high glucose in pancreatic β cells. Biochem. Biophy. Res. Commun, 271, 86-90.
89. [No authors listed] (1993) The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N. Engl. J. Med. 329, 977-986.
90. Greene, D. A., Lattimer, S. A., and Sima, A. A. (1987) Sorbitol, phosphoinositides, and sodium-potassium-ATPase in the pathogenesis of diabetic complications. N. Engl. J. Med. 316, 599-606.
91. Brownlee, M., Cerami, A, and Vlassara, H. (1988) Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. N. Engl. J. Med. 318, 1315-1321.
92. Giugliano, D., Ceriello, A., and Paolisso, G. (1996) Oxidative stress and diabetic vascular complications. Diabetes Care 3, 257-267.
93. Baynes, J. W., and Thorpe, S. R. (1999) Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 48, 1-9.
94. Kunisaki, M., Bursell, S. E., Umeda, F., Nawata, H., and King, G. L. (1994) Normalization of diacylglycerol-protein kinase C activation by vitamin E in aorta of diabetic rats and cultured rat smooth muscle cells exposed to elevated glucose levels. Diabetes 43, 1372-1377.
95. Srivastava, A. K. (2002) High glucose-induced activation of protein kinase signaling pathways in vascular smooth muscle cells: a potential role in the pathogenesis of vascular dysfunction in diabetes. Int. J. Mol. Med. 9, 85-89.
96. Williams, B., Gallacher, B., Patel, H., and Orme, C. (1997) Glucose-induced protein kinase C activation regulates vascular permeability factor mRNA expression and peptide production by human vascular smooth muscle cells in vitro. Diabetes 46, 1497-1503.
97. Ishii, H., Jirousek, M. R., Koya, D., et al. (1996) Amelioration of vascular dysfunctions in diabetic rats by an oral PKC β inhibitor. Science 272, 728-731.
98. Gupta, S., Campbell, D., Derijard, B., and Davis, R. J. (1995) Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science 267, 389-393.
99. Zhang, Z., Apse, K., Pang, J., and Stanton, R. C. (2000) High glucose inhibits glucose-6-phosphate dehydrogenase via cAMP in aortic endothelial cells. J. Biol. Chem. 275, 40042-40047.
100. Erratum in: J. Biol. Chem. (2001) 276, 5412.
101. Yasuda, H., Maeda, K., Sonobe, M., et al. (1994) Metabolic effect of PGE1 analogue 01206α CD on nerve Na(+)-K(+)-ATPase activity of rats with streptozocin-induced diabetes is mediated via cAMP: possible role of cAMP in diabetic neuropathy. Prostaglandins 47, 367-378.
102. Hashim, S., Li, Y., Nagakura, A., Takeo, S., and Anand-Srivastava, M. B. (2004) Modulation of G-protein expression and adenylyl cyclase signaling by high glucose in vascular smooth muscle. Cardiovasc. Res. 63, 709-718.
103. Mancusi, G., Hulter, C., Baumgartner, P. S., Schmidt, K., Schultz, W., and Sexl, V. (1996) High glucose incubaton of human umblican-vein endothelial cells does not alter expression and function either of G protein α-submit or of endothelial O synthase. Biochem. J. 315, 281-287.
104. Tucek, S., Michal, P., and Vlachova, V. (2001) Dual effects of muscarinic M2 receptors on the synthesis of cAMP in CHO cells: background and model. Life Sci. 68, 2501-1510.
105. Anand-Srivastava, M. B., Srivsatava, A. K., and Cantin, M. (1987) Pertussis toxin attenuates atrial natiuretic factor-mediated inhibition of adenylyl cyclase: involvement of inhibitory guanine nucleotide regulatory protein. J. Biol. Chem. 262, 4931-4934.
106. Anand-Srivastava, M. B. (1989) Angiotensin II receptors are negatively coupled to adenylyl cyclase in rat myocardial sarcolemma involvement of inhibitory guanine nucleotide regulatory protein. Biochem. Pharmacol. 38, 489-496.
107. Kook, H., Lee, J. U., Kim, S. W., Kim, S. W., and Baik, Y. H. (2002) Augmented natriuretic peptide-induced guanylyl cyclase activity and vasodilatation in experimental hyperglycemic rats. Jpn. J. Pharmacol. 88, 167-173.
108. Williams, B., Tsai, P., and Schrier, R. W. (1992) Glucose-induced down-regulation of angiotensin II and arginine vasopressin receptors in cultured rat aortic vascular smooth muscles. Role of protein kinase C. J. Clin. Investig. 90, 1992-1999.
109. + channel current in rat small coronary arteries. Circ. Res. 89, 146-152.