Rod Outer Segment Membrane Guanylate Cyclase Type 1 (ROS-GC1) Calcium-modulated Transduction System in the Sperm

Overview

Journal Fertil Steril

Specialty Reproductive Medicine

Date 2008 Dec 30

PMID 19111294

Citations 4

Authors

Anna Jankowska

Beata Burczynska

Teresa Duda

Jerzy B Warchol

Affiliations

Soon will be listed here.

Abstract

Objective: Evaluation of the presence of a Ca(2+)-regulated membrane guanylate cyclase signal transudation system in the spermatozoa.

Design: Experimental study.

Setting: Research university laboratory.

Patient(s): Human sperm obtained from healthy donors who met the criteria of the World Health Organization for normozoospermia and bovine semen collected from bulls of proven fertility.

Intervention(s): Radioimmunoassay and immunohistochemistry of human and bovine spermatozoa.

Main Outcome Measure(s): The membrane guanylate cyclase activity and the presence of membrane guanylate cyclase transduction machinery components in the spermatozoa.

Result(s): The identity of a Ca(2+)-modulated membrane guanylate cyclase transduction machinery in human and bovine spermatozoa has been documented. The machinery is both inhibited and stimulated within nanomolar to semimicromolar range of free Ca(2+). The transduction component of this machinery is the rod outer segment membrane guanylate cyclase type 1 (ROS-GC1). The enzyme coexists with three Ca(2+)-dependent modulators: guanylate cyclase activating protein type 1 (GCAP1), S100B and neurocalcin delta. ROS-GC1 and its modulators are present in the heads and tails of both species' spermatozoa.

Conclusion(s): The coexpression of ROS-GC1 and its activators in spermatozoa suggests that the Ca(2+)-modulated ROS-GC1 transduction system may be a part of the fertilization machinery.

Citing Articles

Transcriptome-wide mA profiling reveals mRNA post-transcriptional modification of boar sperm during cryopreservation.

Qin Z, Wang W, Ali M, Wang Y, Zhang Y, Zhang M BMC Genomics. 2021; 22(1):588.

PMID: 34344298 PMC: 8335898. DOI: 10.1186/s12864-021-07904-8.

Ca(2+)-modulated ROS-GC1 transduction system in testes and its presence in the spermatogenic cells.

Jankowska A, Sharma R, Duda T Front Mol Neurosci. 2014; 7:34.

PMID: 24808824 PMC: 4010774. DOI: 10.3389/fnmol.2014.00034.

Ca(2+)-sensors and ROS-GC: interlocked sensory transduction elements: a review.

Sharma R, Duda T Front Mol Neurosci. 2012; 5:42.

PMID: 22509149 PMC: 3321474. DOI: 10.3389/fnmol.2012.00042.

Ca(2+)-modulated membrane guanylate cyclase in the testes.

Jankowska A, Warchol J Mol Cell Biochem. 2009; 334(1-2):169-79.

PMID: 19915996 DOI: 10.1007/s11010-009-0329-5.

References

Krishnan A, Goraczniak R, Duda T, Sharma R . Third calcium-modulated rod outer segment membrane guanylate cyclase transduction mechanism. Mol Cell Biochem. 1998; 178(1-2):251-9. DOI: 10.1023/a:1006860018300. View

Middendorff R, Muller D, Wichers S, HOLSTEIN A, Davidoff M . Evidence for production and functional activity of nitric oxide in seminiferous tubules and blood vessels of the human testis. J Clin Endocrinol Metab. 1997; 82(12):4154-61. DOI: 10.1210/jcem.82.12.4432. View

Ramarao C, Garbers D . Receptor-mediated regulation of guanylate cyclase activity in spermatozoa. J Biol Chem. 1985; 260(14):8390-6. View

Zhang M, Hong H, Zhou B, Jin S, Wang C, Fu M . The expression of atrial natriuretic peptide in the oviduct and its functions in pig spermatozoa. J Endocrinol. 2006; 189(3):493-507. DOI: 10.1677/joe.1.06483. View

Krishnan A, Venkataraman V, Fik-Rymarkiewicz E, Duda T, Sharma R . Structural, biochemical, and functional characterization of the calcium sensor neurocalcin delta in the inner retinal neurons and its linkage with the rod outer segment membrane guanylate cyclase transduction system. Biochemistry. 2004; 43(10):2708-23. DOI: 10.1021/bi035631v. View

Bohmer M, Van Q, Weyand I, Hagen V, Beyermann M, Matsumoto M . Ca2+ spikes in the flagellum control chemotactic behavior of sperm. EMBO J. 2005; 24(15):2741-52. PMC: 1182239. DOI: 10.1038/sj.emboj.7600744. View

Duda T, Venkataraman V, Krishnan A, Sharma R . Rod outer segment membrane guanylate cyclase type 1 (ROS-GC1) gene: structure, organization and regulation by phorbol ester, a protein kinase C activator. Mol Cell Biochem. 1999; 189(1-2):63-70. DOI: 10.1023/a:1006944629935. View

Duda T, Goraczniak R, Surgucheva I, Gorczyca W, Palczewski K, Sitaramayya A . Calcium modulation of bovine photoreceptor guanylate cyclase. Biochemistry. 1996; 35(26):8478-82. DOI: 10.1021/bi960752z. View

Strunker T, Weyand I, Bonigk W, Van Q, Loogen A, Brown J . A K+-selective cGMP-gated ion channel controls chemosensation of sperm. Nat Cell Biol. 2006; 8(10):1149-54. DOI: 10.1038/ncb1473. View

10.

Aitken R . Molecular mechanisms regulating human sperm function. Mol Hum Reprod. 1997; 3(3):169-73. DOI: 10.1093/molehr/3.3.169. View

11.

Jagannathan S, Punt E, Gu Y, Arnoult C, Sakkas D, Barratt C . Identification and localization of T-type voltage-operated calcium channel subunits in human male germ cells. Expression of multiple isoforms. J Biol Chem. 2001; 277(10):8449-56. DOI: 10.1074/jbc.M105345200. View

12.

Venkataraman V, Duda T, Vardi N, Koch K, Sharma R . Calcium-modulated guanylate cyclase transduction machinery in the photoreceptor--bipolar synaptic region. Biochemistry. 2003; 42(19):5640-8. DOI: 10.1021/bi034025x. View

13.

Duda T, Jankowska A, Venkataraman V, Nagele R, Sharma R . A novel calcium-regulated membrane guanylate cyclase transduction system in the olfactory neuroepithelium. Biochemistry. 2001; 40(40):12067-77. DOI: 10.1021/bi0108406. View

14.

Li H, Ding X, Liao A, Kong X, Xiong C . Expression of CatSper family transcripts in the mouse testis during post-natal development and human ejaculated spermatozoa: relationship to sperm motility. Mol Hum Reprod. 2007; 13(5):299-306. DOI: 10.1093/molehr/gam009. View

15.

Nambi P, Aiyar N, Sharma R . Adrenocorticotropin-dependent particulate guanylate cyclase in rat adrenal and adrenocortical carcinoma: comparison of its properties with soluble guanylate cyclase and its relationship with ACTH-induced steroidogenesis. Arch Biochem Biophys. 1982; 217(2):638-46. DOI: 10.1016/0003-9861(82)90545-8. View

16.

Hinsch K, Hinsch E, Aumuller G, Tychowiecka I, Schultz G, Schill W . Immunological identification of G protein alpha- and beta-subunits in tail membranes of bovine spermatozoa. Biol Reprod. 1992; 47(3):337-46. DOI: 10.1095/biolreprod47.3.337. View

17.

Galindo B, de la Vega-Beltran J, Labarca P, Vacquier V, Darszon A . Sp-tetraKCNG: A novel cyclic nucleotide gated K(+) channel. Biochem Biophys Res Commun. 2007; 354(3):668-75. DOI: 10.1016/j.bbrc.2007.01.035. View

18.

Darszon A, Trevino C, Wood C, Galindo B, Rodriguez-Miranda E, Acevedo J . Ion channels in sperm motility and capacitation. Soc Reprod Fertil Suppl. 2007; 65:229-44. View

19.

Duda T, Venkataraman V, Krishnan A, Nagele R, Sharma R . Negatively calcium-modulated membrane guanylate cyclase signaling system in the rat olfactory bulb. Biochemistry. 2001; 40(15):4654-62. DOI: 10.1021/bi0027985. View

20.

Dizhoor A, Olshevskaya E, Henzel W, Wong S, Stults J, Ankoudinova I . Cloning, sequencing, and expression of a 24-kDa Ca(2+)-binding protein activating photoreceptor guanylyl cyclase. J Biol Chem. 1995; 270(42):25200-6. DOI: 10.1074/jbc.270.42.25200. View