Journal of Yeungnam Medical Science

Yeungnam University College of Medicine, Yeungnam University Institute Medical Science (영남대 의대 학술지 편집위원회)
권호 표지
DOI QR코드

DOI QR Code

Sulfatase 1 mediates the inhibitory effect of angiotensin II type 2 receptor inhibitor on angiotensin II-induced hypertensive mediator expression and proliferation in vascular smooth muscle cells from spontaneously hypertensive rats

  • Kim, Hye Young (Department of Microbiology, Yeungnam University College of Medicine) ;
  • Cha, Hye Ju (Department of Microbiology, Yeungnam University College of Medicine) ;
  • Kim, Hee Sun (Department of Microbiology, Yeungnam University College of Medicine)
  • Received : 2017.04.26
  • Accepted : 2017.05.22
  • Published : 2017.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Extracellular sulfatases (Sulfs), sulfatase 1 (Sulf1) and sulfatase 2 (Sulf2), play a pivotal role in cell signaling by remodeling the 6-O-sulfation of heparan sulfate proteoglycans on the cell surface. The present study examined the effects of Sulfs on angiotensin II (Ang II)-induced hypertensive mediator expression and vascular smooth muscle cells (VSMCs) proliferation in spontaneously hypertensive rats (SHR). Methods: Ang II receptors, 12-lipoxygenase (12-LO), and endothelin-1 (ET-1) messenger RNA (mRNA) expressions in SHR VSMCs were analyzed by real-time polymerase chain reaction and Western blotting. VSMCs proliferation was determined by [$^3H$]-thymidine incorporation. Results: Basal Sulfs mRNAs expression and enzyme activity were elevated in SHR VSMCs. However, Sulfs had no effect on the basal or Ang II-induced 12-LO and ET-1 mRNA expression in SHR VSMCs. The inhibition of Ang II-induced 12-LO and ET-1 expression by blockade of the Ang II type 2 receptor ($AT_2\;R$) pathway was not observed in Sulf1 siRNA-transfected SHR VSMCs. However, Sulf2 did not affect the action of $AT_2\;R$ inhibitor on Ang II-induced 12-LO and ET-1 expression in SHR VSMCs. The down-regulation of Sulf1 induced a reduction of $AT_2\;R$ mRNA expression in SHR VSMCs. In addition, the inhibition of Ang II-induced VSMCs proliferation by blockade of the $AT_2\;R$ pathway was mediated by Sulf1 in SHR VSMCs. Conclusion: These findings suggest that extracellular sulfatase Sulf1 plays a modulatory role in the $AT_2\;R$ pathway that leads to an Ang II-induced hypertensive effects in SHR VSMCs.

Keywords

References

  1. Buono M, Cosma MP. Sulfatase activities towards the regulation of cell metabolism and signaling in mammals. Cell Mol Life Sci 2010;67:769-80. https://doi.org/10.1007/s00018-009-0203-3
  2. Sardiello M, Annunziata I, Roma G, Ballabio A. Sulfatases and sulfatase modifying factors: an exclusive and promiscuous relationship. Hum Mol Genet 2005;14:3203-17. https://doi.org/10.1093/hmg/ddi351
  3. Nagamine S, Koike S, Keino-Masu K, Masu M. Expression of a heparan sulfate remodeling enzyme, heparan sulfate 6-Oendosulfatase sulfatase FP2, in the rat nervous system. Brain Res Dev Brain Res 2005;159:135-43. https://doi.org/10.1016/j.devbrainres.2005.07.006
  4. Morimoto-Tomita M, Uchimura K, Werb Z, Hemmerich S, Rosen SD. Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans. J Biol Chem 2002;277(51):49175-85. https://doi.org/10.1074/jbc.M205131200
  5. Honke K, Taniguchi N. Sulfotransferases and sulfated oligosaccharides. Med Res Rev 2002;22:637-54. https://doi.org/10.1002/med.10020
  6. Langsdorf A, Do AT, Kusche-Gullberg M, Emerson CP Jr, Ai X. Sulfs are regulators of growth factor signaling for satellite cell differentiation and muscle regeneration. Dev Biol 2007;311:464-77. https://doi.org/10.1016/j.ydbio.2007.08.053
  7. Dai Y, Yang Y, MacLeod V, Yue X, Rapraeger AC, Shriver Z, et al. HSulf-1 and HSulf-2 are potent inhibitors of myeloma tumor growth in vivo. J Biol Chem 2005;280(48):40066-73. https://doi.org/10.1074/jbc.M508136200
  8. Holst CR, Bou-Reslan H, Gore BB, Wong K, Grant D, Chalasani S, et al. Secreted sulfatases Sulf1 and Sulf2 have overlapping yet essential roles in mouse neonatal survival. PLoS One 2007;2:e575. https://doi.org/10.1371/journal.pone.0000575
  9. Ratzka A, Kalus I, Moser M, Dierks T, Mundlos S, Vortkamp A. Redundant function of the heparan sulfate 6-O-endosulfatases Sulf1 and Sulf2 during skeletal development. Dev Dyn 2008;237:339-53. https://doi.org/10.1002/dvdy.21423
  10. Narita K, Staub J, Chien J, Meyer K, Bauer M, Friedl A, et al. HSulf-1 inhibits angiogenesis and tumorigenesis in vivo. Cancer Res 2006;66:6025-32. https://doi.org/10.1158/0008-5472.CAN-05-3582
  11. Zhang H, Newman DR, Sannes PL. HSULF-1 inhibits ERK and AKT signaling and decreases cell viability in vitro in human lung epithelial cells. Respir Res 2012;13:69. https://doi.org/10.1186/1465-9921-13-69
  12. Morimoto-Tomita M, Uchimura K, Bistrup A, Lum DH, Egeblad M, Boudreau N, et al. Sulf-2, a proangiogenic heparan sulfate endosulfatase, is upregulated in breast cancer. Neoplasia 2005;7:1001-10. https://doi.org/10.1593/neo.05496
  13. Uchimura K, Morimoto-Tomita M, Bistrup A, Li J, Lyon M, Gallagher J, et al. HSulf-2, an extracellular endoglucosamine- 6-sulfatase, selectively mobilizes heparin-bound growth factors and chemokines: effects on VEGF, FGF-1, and SDF-1. BMC Biochem 2006;7:2. https://doi.org/10.1186/1471-2091-7-2
  14. Heintz B, Stöcker G, Mrowka C, Rentz U, Melzer H, Stickeler E, et al. Decreased glomerular basement membrane heparan sulfate proteoglycan in essential hypertension. Hypertension 1995;25:399-407. https://doi.org/10.1161/01.HYP.25.3.399
  15. Sala-Newby GB, George SJ, Bond M, Dhoot GK, Newby AC. Regulation of vascular smooth muscle cell proliferation, migration and death by heparan sulfate 6-O-endosulfatase1. FEBS Lett 2005;579:6493-8. https://doi.org/10.1016/j.febslet.2005.10.026
  16. Kim HY, Kang YJ, Song IH, Choi HC, Kim HS. Upregulation of interleukin-8/CXCL8 in vascular smooth muscle cells from spontaneously hypertensive rats. Hypertens Res 2008;31: 515-23. https://doi.org/10.1291/hypres.31.515
  17. Kim JH, Kim HS. Downregulation of angiotensin II-induced 12-lipoxygenase expression and cell proliferation in vascular smooth muscle cells from spontaneously hypertensive rats by CCL5. Korean J Physiol Pharmacol 2009;13:385-92. https://doi.org/10.4196/kjpp.2009.13.5.385
  18. Kim HY, Choi JH, Kang YJ, Park SY, Choi HC, Kim HS. Reparixin, an inhibitor of CXCR1 and CXCR2 receptor activation, attenuates blood pressure and hypertension-related mediators expression in spontaneously hypertensive rats. Biol Pharm Bull 2011;34:120-7. https://doi.org/10.1248/bpb.34.120
  19. Otsuki S, Taniguchi N, Grogan SP, D'Lima D, Kinoshita M, Lotz M. Expression of novel extracellular sulfatases Sulf-1 and Sulf-2 in normal and osteoarthritic articular cartilage. Arthritis Res Ther 2008;10:R61. https://doi.org/10.1186/ar2432
  20. Tsai TT, Ho NY, Fang HC, Lai PL, Niu CC, Chen LH, et al. Increased sulfatase 1 gene expression in degenerative intervertebral disc cells. J Orthop Res 2015;33:312-7. https://doi.org/10.1002/jor.22766
  21. Sasaki M, Hori MT, Hino T, Golub MS, Tuck ML. Elevated 12-lipoxygenase activity in the spontaneously hypertensive rat. Am J Hypertens 1997;10:371-8.
  22. Wu R, Millette E, Wu L, de Champlain J. Enhanced superoxide anion formation in vascular tissues from spontaneously hypertensive and desoxycorticosterone acetate-salt hypertensive rats. J Hypertens 2001;19:741-8. https://doi.org/10.1097/00004872-200104000-00011
  23. Kim HY, Jeong DW, Park HS, Lee TY, Kim HS. Comparison of 12-lipoxygenase expression in vascular smooth muscle cells from old normotensive Wistar-Kyoto rats with spontaneously hypertensive rats. Hypertens Res 2013;36:65-73. https://doi.org/10.1038/hr.2012.119
  24. Horiuchi M, Lehtonen JY, Daviet L. Signaling mechanism of the AT2 angiotensin II receptor: crosstalk between AT1 and AT2 receptors in cell growth. Trends Endocrinol Metab 1999;10:391-6. https://doi.org/10.1016/S1043-2760(99)00191-5
  25. Guo F, Chen XL, Wang F, Liang X, Sun YX, Wang YJ. Role of angiotensin II type 1 receptor in angiotensin II-induced cytokine production in macrophages. J Interferon Cytokine Res 2011;31:351-61. https://doi.org/10.1089/jir.2010.0073
  26. Kim HY, Cha HJ, Kim HS. CCL5 upregulates activation of AMP-activated protein kinases in vascular smooth muscle cells of spontaneously hypertensive rats. Cytokine 2014;67:77-84. https://doi.org/10.1016/j.cyto.2014.02.010
  27. Kim HY, Kim HS. Dimethylarginine dimethylaminohydrolase- 1 mediates inhibitory effect of interleukin-10 on angiotensin II-induced hypertensive effects in vascular smooth muscle cells of spontaneously hypertensive rats. Cytokine 2016;77: 203-10. https://doi.org/10.1016/j.cyto.2015.09.002
  28. Kim HY, Kim JH, Kim HS. Effect of CCL5 on dimethylarginine dimethylaminohydrolase-1 production in vascular smooth muscle cells from spontaneously hypertensive rats. Cytokine 2013;64:227-33. https://doi.org/10.1016/j.cyto.2013.06.316
  29. Li J, Mo ML, Chen Z, Yang J, Li QS, Wang DJ, et al. HSulf-1 inhibits cell proliferation and invasion in human gastric cancer. Cancer Sci 2011;102:1815-21. https://doi.org/10.1111/j.1349-7006.2011.02024.x
  30. Liu CT, Zhu ST, Li P, Wang YJ, Zhang H, Zhang ST. SULF1 inhibits proliferation and invasion of esophageal squamous cell carcinoma cells by decreasing heparin-binding growth factor signaling. Dig Dis Sci 2013;58:1256-63. https://doi.org/10.1007/s10620-012-2429-4
  31. Yang JD, Sun Z, Hu C, Lai J, Dove R, Nakamura I, et al. Sulfatase 1 and sulfatase 2 in hepatocellular carcinoma: associated signaling pathways, tumor phenotypes, and survival. Genes Chromosomes Cancer 2011;50:122-35. https://doi.org/10.1002/gcc.20838
  32. Lai JP, Sandhu DS, Yu C, Han T, Moser CD, Jackson KK, et al. Sulfatase 2 up-regulates glypican 3, promotes fibroblast growth factor signaling, and decreases survival in hepatocellular carcinoma. Hepatology 2008;47:1211-22. https://doi.org/10.1002/hep.22202