Skip to main content
SpringerLink
Log in

Odorant-linked ROS-GC subfamily membrane guanylate cyclase transduction system

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

This review focuses on the principles of the Ca2+-modulated ROS-GC subfamily transduction system linked with the mammalian olfactory transduction field, its historical development, and the present day status on its constitution and operational mechanisms controlling the process of olfactory-transduction. Beginning parts of this article are freely borrowed from the earlier reviews of the authors (Sharma RK, Duda T, Venkataraman V, Koch KW, Curr Topics Biochem Res 6:111–144, 2004; Duda T, Venkataraman V, Sharma RK, Neuronal calcium sensor proteins, pp 91–113, Nova Science Publishers, Inc., 2007).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Beets MG (1970) The molecular parameters of olfactory response. Pharmacol Rev 22:1–34

    CAS  PubMed  Google Scholar 

  2. Bossert WH, Wilson EO (1963) The analysis of olfactory communication among animals. J Theor Biol 5:443–469

    Article  CAS  PubMed  Google Scholar 

  3. Buck LB (1996) Information coding in the vertebrate olfactory system. Ann Rev Neurosci 19:517–544

    Article  CAS  PubMed  Google Scholar 

  4. Buck LB (2000) The molecular architecture of odor and pheromone sensing in mammals. Cell 100:611–618

    Article  CAS  PubMed  Google Scholar 

  5. Doty RL (2001) Olfaction. Annu Rev Psychol 52:423–452

  6. Halpern M (1987) The organization and function of the vomeronasal system. Ann Rev Neurosci. 10:325–362

    Article  CAS  PubMed  Google Scholar 

  7. Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Ann Rev Neurosci 20:595–631

    Article  CAS  PubMed  Google Scholar 

  8. Duda T, Venkataraman V, Krishnan A, Nagele RG, Sharma RK (2001) Negatively calcium-modulated membrane guanylate cyclase signaling system in the rat olfactory bulb. Biochemistry 40:4654–4662

    Article  CAS  PubMed  Google Scholar 

  9. Venkataraman V, Nagele R, Duda T, Sharma RK (2000) Rod outer segment membrane guanylate cyclase type 1-linked stimulatory and inhibitory calcium signaling systems in the pineal gland: biochemical, molecular, and immunohistochemical evidence. Biochemistry 39:6042–6052

    Article  CAS  PubMed  Google Scholar 

  10. Shepherd GM, Greer CA (1998) Olfactory bulb. In: Shepherd GM (ed) The synaptic organization of the brain. Oxford University Press, New York, pp 159–203

    Google Scholar 

  11. Pinching AJ, Powell TP (1971) The neuron types of the glomerular layer of the olfactory bulb. J Cell Sci 9:305–345

    CAS  PubMed  Google Scholar 

  12. Hwang JY, Lange C, Helten A, Höppner-Heitmann D, Duda T, Sharma RK, Koch KW (2003) Regulatory modes of rod outer segment membrane guanylate cyclase differ in catalytic efficiency and Ca(2+)-sensitivity. Eur J Biochem 270:3814–3821

    Article  CAS  PubMed  Google Scholar 

  13. Sharma RK, Duda T, Venkataraman V, Koch KW (2004) Calcium-modulated membrane guanylate cyclase ROS-GC transduction machinery in sensory neurons: a universal concept. Curr Topics Biochem Res 6:111–144

    CAS  Google Scholar 

  14. Sharma RK, Duda T (2006) Calcium sensor neurocalcin δ-modulated ROS-GC transduction machinery in the retinal and olfactory neurons. Calcium Binding Proteins 1:7–11

    CAS  Google Scholar 

  15. Duda T, Fik-Rymarkiewicz E, Venkataraman V, Krishnan A, Sharma RK (2004) Calcium-modulated ciliary membrane guanylate cyclase transduction machinery: constitution and operational principles. Mol Cell Biochem 267:107–122

    Article  CAS  PubMed  Google Scholar 

  16. Duda T, Venkataraman V, Sharma RK (2007) Constitutional and operational principles of the retinal and odorant-linked neurocalcin δ-dependent Ca2+ modulated ROS-GC machinery. In: Philipov P, Koch KW (eds) Neuronal calcium sensor proteins. Nova Science Publishers, Inc., Hauppauge, NY, pp 91–113

    Google Scholar 

  17. Belluscio L, Gold GH, Nemes A, Axel R (1998) Mice deficient in G(olf) are anosmic. Neuron 20:69–81

    Article  CAS  PubMed  Google Scholar 

  18. Breer H (2003) Olfactory receptors: molecular basis for recognition and discrimination of odors. Anal Bioanal Chem 377:427–433

    Article  CAS  PubMed  Google Scholar 

  19. Buck LB (2000) The molecular architecture of odor and pheromone sensing in mammals. Cell 100:611–618

    Article  CAS  PubMed  Google Scholar 

  20. Buck LB (1995) Unraveling chemosensory diversity. Cell 83:349–352

    Article  CAS  PubMed  Google Scholar 

  21. Lai PC, Singer MS, Crasto CJ (2005) Structural activation pathways from dynamic olfactory receptor-odorant interactions. Chem Senses 30:781–792

    Article  CAS  PubMed  Google Scholar 

  22. Fulle HJ, Vassar R, Foster DC, Yang RB, Axel R, Garbers DL (1995) A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons. Proc Natl Acad Sci USA 92:3571–3575

    Article  CAS  PubMed  Google Scholar 

  23. Juilfs DM, Fulle HJ, Zhao AZ, Houslay MD, Garbers DL, Beavo JA (1997) A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase-D define a unique olfactory signal transduction pathway. Proc Natl Acad Sci USA 9:3388–3395

    Article  Google Scholar 

  24. Meyer MR, Angele A, Kremmer E, Kaupp UB, Muller F (2000) A cGMP-signaling pathway in a subset of olfactory sensory neurons. Proc Natl Acad Sci USA 97:10595–10600

    Article  CAS  PubMed  Google Scholar 

  25. Duda T, Jankowska A, Venkataraman V, Nagele RG, Sharma RK (2001) A novel calcium-regulated membrane guanylate cyclase transduction system in the olfactory neuroepithelium. Biochemistry 40:12067–12077

    Article  CAS  PubMed  Google Scholar 

  26. Duda T, Krishnan R, Sharma RK (2006) GCAP1: antithetical calcium sensor of ROS-GC transduction machinery. Calcium Binding Proteins 1:102–107

    Google Scholar 

  27. Kaupp UB, Seifert R (2002) Cyclic nucleotide-gated ion channels. Physiol Rev 82:769–824

    CAS  PubMed  Google Scholar 

  28. Leinders-Zufall T, Cockerham RE, Michalakis S, Biel M, Garbers DL, Reed RR, Zufall F, Munger SD (2007) Contribution of the receptor guanylyl cyclase GC-D to chemosensory function in the olfactory epithelium. Proc Natl Acad Sci USA 104:14507–14512

    Article  CAS  PubMed  Google Scholar 

  29. Teicher MH, Stewart WB, Kauer JS, Shepherd GM (1980) Suckling pheromone stimulation of a modified glomerular region in the developing rat olfactory bulb revealed by the 2-deoxyglucose method. Brain Res 194:530–535

    Article  CAS  PubMed  Google Scholar 

  30. Greer CA, Stewart WB, Teicher MH, Shepherd GM (1982) Functional development of the olfactory bulb and a unique glomerular complex in the neonatal rat. J Neurosci 2:1744–1759

    CAS  PubMed  Google Scholar 

  31. Yagi T, Aizawa S, Tokunaga T, Shigetani Y, Takeda N, Ikawa Y (1993) A role for Fyn tyrosine kinase in the suckling behaviour of neonatal mice. Nature 366:742–745

    Article  CAS  PubMed  Google Scholar 

  32. Duda T, Sharma RK (2008) ONE-GC membrane guanylate cyclase, a trimodal odorant signal transducer. Biochem Biophys Res Commun 367:440–445

    Article  CAS  PubMed  Google Scholar 

  33. Wilson EM, Chinkers M (1995) Identification of sequences mediating guanylyl cyclase dimerization. Biochemistry 34:4696–4701

    Article  CAS  PubMed  Google Scholar 

  34. Ramamurthy V, Tucker C, Wilkie SE, Daggett V, Hunt DM, Hurley J (2001) Interactions within the coiled-coil domain of RetGC-1 guanylyl cyclase are optimized for regulation rather than for high affinity. J Biol Chem 276:26218–26229

    Article  CAS  PubMed  Google Scholar 

  35. Duda T, Sharma RK (2009) Ca2+-modulated ONE-GC odorant signal transduction. FEBS Lett 583:1327–1330

    Article  CAS  PubMed  Google Scholar 

  36. Munger SD, Leinders-Zufall T, Zufall F (2009) Subsystem organization of the mammalian sense of smell. Annu Rev Physiol 71:115–140

    Google Scholar 

  37. Krishnan A, Duda T, Pertzev A, Kobayashi M, Takamatsu K, Sharma RK (2009) Hippocalcin, new Ca(2+) sensor of a ROS-GC subfamily member, ONE-GC, membrane guanylate cyclase transduction system. Mol Cell Biochem 325:1–14

    Article  CAS  PubMed  Google Scholar 

  38. Caenepeel S, Charydczak G, Sudarsanam S, Hunter T, Manning G (2004) The mouse kinome: discovery and comparative genomics of all mouse protein kinases. Proc Natl Acad Sci USA 101:11707–11712

    Article  CAS  PubMed  Google Scholar 

  39. Fik-Rymarkiewicz E, Duda T, Sharma RK (2006) Novel frequenin-modulated Ca2+-signaling membrane guanylate cyclase (ROS-GC) transduction pathway in bovine hippocampus. Mol Cell Biochem 291:187–204

    Article  CAS  PubMed  Google Scholar 

  40. Paul AK, Marala RB, Jaiswal RK, Sharma RK (1987) Coexistence of guanylate cyclase and atrial natriuretic factor receptor in a 180-kD protein. Science 235:1224–1226

    Article  CAS  PubMed  Google Scholar 

  41. Hu J, Zhong C, Ding C, Chi Q, Walz A, Mombaerts P, Matsunami H, Luo M (2007) Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse. Science 317:953–957

    Article  CAS  PubMed  Google Scholar 

  42. Sun L, Wang H, Hu J, Han J, Matsunami H, Luo M (2009) Guanylyl cyclase-D in the olfactory CO2 neurons is activated by bicarbonate. Proc Natl Acad Sci USA 106:2041–2046

    Article  CAS  PubMed  Google Scholar 

  43. Guo D, Zhang JJ, Huang XY (2009) Stimulation of guanylyl cyclase-D by bicarbonate. Biochemistry 48:4417–4422

    Article  CAS  PubMed  Google Scholar 

  44. Fleischer J, Mamasuew K, Breer H (2009) Expression of cGMP signaling elements in the Grueneberg ganglion. Histochem Cell Biol 131:75–88

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgment

This research was supported by USPHS awards: DC 005349 (R.K.S.), HL 084584 (T.D.).

Author information

Authors and Affiliations

  1. Research Divisions of Biochemistry and Molecular Biology, The Unit of Regulatory and Molecular Biology, Salus University, Elkins Park, PA, 19027, USA

    Rameshwar K. Sharma & Teresa Duda

Authors
  1. Rameshwar K. Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Teresa Duda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rameshwar K. Sharma.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sharma, R.K., Duda, T. Odorant-linked ROS-GC subfamily membrane guanylate cyclase transduction system. Mol Cell Biochem 334, 181–189 (2010). https://doi.org/10.1007/s11010-009-0333-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-009-0333-9

Keywords

Search

Navigation