Share This Article:

Age dependent expression and distribution of nitric oxide (NO) synthase isoforms in the ovine kidney

Full-Text HTML Download Download as PDF (Size:2341KB) PP. 61-70
DOI: 10.4236/ojmip.2013.32010    3,538 Downloads   6,132 Views   Citations

ABSTRACT

The aim of the present study was to measure intrarenal spatial and temporal localization of all three nitric oxide synthase (NOS) isoforms in the developing ovine kidney. Reverse transcriptase-polymerase chain reaction (RT-PCR), Western Blot analyses, and in situ hybridization techniques were performed for NOS I -III isoforms in renal tissue obtained from sheep aged ~24 h, one, three, six, and 12 weeks post natally (N = 3). RT-PCR performed on cortical and medullary kidney tissue revealed the presence of all three NOS isoforms from day one to 12 weeks postnatally. NOS I and NOS II mRNA levels were greater in cortex compared to medulla during the first three weeks whereas NOS III mRNA levels were predominantly transcribed within the medulla. In all NOS isoforms, there was a decrease in cortical mRNA levels after three to six weeks. Protein levels confirmed the presence of all three NOS isoforms over the first three months of postnatal life. By demonstrating NOS isoform transcripts to be more abundant in the early post natal period, these findings may provide insight into the age dependent role of NO in modulating kidney function during ontogeny.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

Davis, D. , Lewis, M. , Qi, W. , Hart, D. and Smith, F. (2013) Age dependent expression and distribution of nitric oxide (NO) synthase isoforms in the ovine kidney. Open Journal of Molecular and Integrative Physiology, 3, 61-70. doi: 10.4236/ojmip.2013.32010.

References

[1] Kone, B.C., Kuncewicz, T., Zhang, W. and Yu, Z.Y. (2003) Protein interactions with nitric oxide synthases: Controlling the right time, the right place, and the right amount of nitric oxide. American Journal of Physiology. Renal Physiology, 285, F178-F190.
[2] Sener, A. and Smith, F.G. (2001) Nitric oxide modulates the arterial baroreflex control of heart rate in conscious lambs in an age-dependent manner. American Journal of Physiology. Heart and Circulatory Physiology, 280, 2255-2263.
[3] Sener, A. and Smith, F.G. (2001) Renal hemodynamic effects of L-NAME during postnatal maturation in conscious lambs. Pediatric Nephrology, 16, 868-873. doi:10.1007/s004670100672
[4] Sener, A. and Smith, F.G. (1999) Dose dependent effects of nitric oxide synthase inhibition on systemic and renal haemodynamics in conscious lambs. Canadian Journal of Physiology and Pharmacology, 77, 1-7. doi:10.1139/y99-009
[5] Sener, A. and Smith, F.G. (2002) Glomerular and tubular responses to NG-nitro-L-arginine methyl ester are age dependent in conscious lambs. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 282, R1512-R1520.
[6] Solhaug, M.J., Dong, X.Q., Adelman, R.D. and Dong, K.W. (2000) Ontogeny of neuronal nitric oxide synthase, NOS I, in the developing porcine kidney. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 278, R1453-R1459.
[7] Solhaug, M.J., Kullaprawithaya, U., Dong, X.Q. and Dong, K.-W. (2001) Expression of endothelial nitric oxide synthase in the postnatal developing porcine kidney. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 280, R1269-R1275.
[8] Fischer, E., Schnermann, J., Briggs, J.P., Kriz, W., Ronco, P.M. and Bachmann, S. (1995) Ontogeny of NO synthase and renin in juxtaglomerular apparatus of rat kidneys. American Journal of Physiology, 268, F1164-F1176.
[9] Han, K.-H., Lim, J.-M., Kim, W.-Y., Kim, H., Madsen, K.M. and Kim, J. (2005) Expression of endothelial nitric oxide synthase in developing rat kidney. American Journal of Physiology. Renal Physiology, 288, F694-F702. doi:10.1152/ajprenal.00085.2004
[10] Reno, C., Marchuk, L., Sciore, P., Frank, C.B. and Hart, D.A. (1997) Rapid isolation of total RNA from small samples of hypocellular, dense connective tissues. Bio-Techniques, 22, 1082-1086.
[11] Le Graverand, M.-P.H., Eggerer, J., Sciore, P., Reno, C., Vignon, E., Otterness, I. and Hart, D.A. (2000) Matrix metalloproteinase-13 expression in rabbit knee joint connective tissues: Influence of maturation and response to injury. Matrix Biology, 19, 431-441. doi:10.1016/S0945-053X(00)00093-7
[12] Sciore, P., Frank, C.B. and Hart, D.A. (1998) Identification of sex hormone receptors in human and rabbit ligaments of the knee by reverse transcription-polymerase chain reaction: Evidence that receptors are present in tis- sue from both male and female subjects. Journal of Orthopaedic Research, 16, 604-610. doi:10.1002/jor.1100160513
[13] Marchuk, L., Sciore, P., Reno, C., Frank, C.B. and Hart, D.A. (1998) Postmortem stability of total RNA isolated from rabbit ligament, tendon and cartilage. Biochimica et Biophysica Acta (BBA)—General Subjects, 1379, 171-177. doi:10.1016/S0304-4165(97)00094-9
[14] Berglund, M., Wiig, M., Torstensson, M., Reno, C. and Hart, D.A. (2004) Assessment of mRNA levels for matrix molecules and TGF-beta1 in rabbit flexor and peroneus tendons reveals regional differences in steady-state expression. Journal of Hand Surgery, 29, 165-169. doi:10.1016/j.jhsb.2003.09.005
[15] Forstermann, U., Closs, E.I., Pollock, J.S., Nakane, M., Schwarz, P., Gath, I. and Kleinert, H. (1994) Nitric oxide synthase isozymes. Characterization, purification, molecular cloning, and functions. Hypertension, 23, 1121-1131. doi:10.1161/01.HYP.23.6.1121
[16] Forstermann, U., Pollock, J.S., Tracey, W.R. and Nakane, M. (1994) Isoforms of nitric-oxide synthase: Purification and regulation. Methods in Enzymology, 233, 258-264. doi:10.1016/S0076-6879(94)33029-8
[17] Trifonov, S., Houtani, T., Hamada, S., Kase, M., Maruyama, M. and Sugimoto, T. (2009) In situ hybridization study of the distribution of choline acetyltransferase mRNA and its splice variants in the mouse brain and spinal cord. Neuroscience, 159, 344-357. doi:10.1016/j.neuroscience.2008.12.054
[18] Moningka, N.C., Sindler, A.L., Muller-Delp, J.M. and Baylis, C. (2011) Twelve weeks of treadmill exercise does not alter age-dependent chronic kidney disease in the Fisher 344 male rat. The Journal of Physiology, 589, 6129-6138.
[19] Schwartz, D., Mendonca, M., Schwartz, I., Xia, Y., Satriano, J., Wilson, C.B. and Blantz, R.C. (1997) Inhibition of constitutive nitric oxide synthase (NOS) by nitric oxide generated by inducible NOS after lipopolysaccharide administration provokes renal dysfunction in rats. The Journal of Clinical Investigation, 100, 439-448. doi:10.1172/JCI119551
[20] Cattell, V. (2002) Nitric oxide and glomerulonephritis. Kidney International, 61, 816-821. doi:10.1046/j.1523-1755.2002.00226.x
[21] Blantz, R.C., Deng, A., Lortie, M., Munger, K., Vallon, V., Gabbai, F.B. and Thomson, S.C. (2002) The complex role of nitric oxide in the regulation of glomerular ultrafiltration. Kidney International, 61, 782-785. doi:10.1046/j.1523-1755.2002.00220.x
[22] Mount, P.F. and Power, D.A. (2006) Nitric oxide in the kidney: Functions and regulation of synthesis. Acta Physiologica, 187, 433-446. doi:10.1111/j.1748-1716.2006.01582.x
[23] Kone, B.C. (2004) Nitric oxide synthesis in the kidney: Isoforms, biosynthesis, and functions in health. Seminars in Nephrology, 24, 299-315. doi:10.1016/j.semnephrol.2004.04.002
[24] Kone, B.C. (1999) Localization and regulation of nitric oxide synthase isoforms in the kidney. Seminars in Nephrology, 19, 230-241.
[25] Wu, F., Park, F., Cowley Jr., A.W. and Mattson, D.L. (1999) Quantification of nitric oxide synthase activity in microdissected segments of the rat kidney. American Journal of Physiology, 276, F874-F881.
[26] Mattson, D.L. and Wu, F. (2000) Nitric oxide synthase activity and isoforms in rat renal vasculature. Hypertension, 35, 337-341. doi:10.1161/01.HYP.35.1.337
[27] Sullivan, J.C., Pardieck, J.L., Hyndman, K.A. and Pollock, J.S. (2010) Renal NOS activity, expression, and localization in male and female spontaneously hypertensive rats. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 298, R61-R69. doi:10.1152/ajpregu.00526.2009
[28] Bachmann, S., Bosse, H.M. and Mundel, P. (1995) Topography of nitric oxide synthesis by localizing constitutive NO synthases in mammalian kidney. American Journal of Physiology, 268, F885-F898.
[29] Mattson, D.L. and Bellehumeur, T.G. (1996) Neural nitric oxide synthase in the renal medulla and blood pressure regulation. Hypertension, 28, 297-303. doi:10.1161/01.HYP.28.2.297
[30] Liu, L., Liu, G.L. and Barajas, L. (1996) Distribution of nitric oxide synthase-containing ganglionic neuronal somata and postganglionic fibers in the rat kidney. Journal of Comparative Neurology, 369, 16-30. doi:10.1002/(SICI)1096-9861(19960520)369:1<16::AID-CNE2>3.0.CO;2-N
[31] Wilcox, C.S. (1998) Role of macula densa NOS in tubuloglomerular feedback. Current Opinion in Nephrology and Hypertension, 7, 443-449. doi:10.1097/00041552-199807000-00016
[32] Garvin, J.L. and Hong, N.J. (1999) Nitric oxide inhibits sodium-hydrogen exchange activity in the thick ascending limb. American Journal of Physiology, 277, F377-F382.
[33] Stoos, B.A., Garcia, N.H. and Garvin, J.L. (1995) Nitric oxide inhibits sodium reabsorption in the isolated perfused cortical collecting duct. Journal of the American Society of Nephrology, 6, 89-94.
[34] Adler, S., Huang, H., Loke, K.E., Xu, X., Tada, H., Laumas, A. and Hintze, T.H. (2001) Endothelial nitric oxide synthase plays an essential role in regulation of renal oxygen consumption by NO. American Journal of Physiology—Renal Physiology, 280, F838-F843.
[35] Plato, C.F., Stoos, B.A., Wang, D. and Garvin, J.L. (1999) Endogenous nitric oxide inhibits chloride transport in the thick ascending limb. American Journal of Physiology, 276, F159-F163.
[36] Holmqvist, B., Olsson, C.F., Svensson, M.L., Svanborg, C., Forsell, J. and Alm, P. (2005) Expression of nitric oxide synthase isoforms in the mouse kidney: Cellular localization and influence by lipopolysaccharide and tolllike receptor 4. Journal of Molecular Histology, 36, 499-516. doi:10.1007/s10735-006-9028-7
[37] Ahn, K.Y., Mohaupt, M.G., Madsen, K.M. and Kone, B.C. (1994) In situ hybridization localization of mRNA encoding inducible nitric oxide synthase in rat kidney. American Journal of Physiology, 267, F748-F757.
[38] Morrissey, J.J., McCracken, R., Kaneto, H., Vehaskari, M., Montani, D. and Klahr, S. (1994) Location of an inducible nitric oxide synthase mRNA in the normal kidney. Kidney International, 45, 998-1005. doi:10.1038/ki.1994.135
[39] Munger, K.A., Blantz, R.C. and Lortie, M.J. (2006) Acute renal response to LPS: impaired arginine production and inducible nitric oxide synthase activity. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 291, R684-R691. doi:10.1152/ajpregu.00873.2005
[40] Parker, T.A., Le Cras, T.D., Kinsella, J.P. and Abman, S.H. (2000) Developmental changes in endothelial nitric oxide synthase expression and activity in ovine fetal lung. American Journal of Physiology—Lung Cellular and Molecular Physiology, 278, L202-L208.
[41] Monau, T.R., Vargas, V.E., King, N., Yellon, S.M., Myers, D.A. and Ducsay, C.A. (2009) Long-term hypoxia increases endothelial nitric oxide synthase expression in the ovine fetal adrenal. Reproduction Science, 16, 865-874. doi:10.1177/1933719109336678
[42] Khan, H., Kusakabe, K.T., Wakitani, S., Hiyama, M., Takeshita, A. and Kiso, Y. (2011) Expression and localization of NO synthase isoenzymes (iNOS and eNOS) in development of the rabbit placenta. Journal of Reproduction and Development, 58, 231-236.
[43] Sener, A. and Smith, F.G. (1999) Acetylcholine chloride and renal haemodynamics during postnatal maturation in conscious lambs. Journal of Applied Physiology, 87, 1296-1300.
[44] Smith, F.G., van der Velde, L. and Sener, A. (2005) Nitric oxide modulates renal vasoconstrictor effect of endothelin1 in conscious lambs. Pediatric Nephrology, 20, 1545-1551. doi:10.1007/s00467-005-2015-5

  
comments powered by Disqus

Copyright © 2018 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.