Skip to main content

Advertisement

SpringerLink
Log in

Decreased Retinal Neuronal Cell Death in Caspase-1 Knockout Mice

  • LABORATORY INVESTIGATION
  • Published:
Japanese Journal of Ophthalmology Aims and scope Submit manuscript

Abstract

Purpose

To determine whether apoptosis of retinal neurons induced by excessive light exposure and ischemia–reperfusion injury is altered in caspase-1 knockout mice.

Methods

Eight- to 10-week-old caspase-1 knockout mice (Casp1–/–) and wild-type (WT) mice (C57BL/6) were exposed to diffuse, cool, white fluorescent light of 25 000 lux for 2 h. Other mice were subjected to retinal ischemia by increasing the intraocular pressure to 110 mmHg for 45 min. Electroretinograms (ERGs) were recorded before and after the light exposure. TdT-dUTP terminal nick-end labeling (TUNEL) was performed to identify the apoptotic cells after the insults. The inner retinal thickness was measured to evaluate the retinal injury after the ischemia–reperfusion. Expression of caspase-1 protein was studied by immunohistochemical analysis and Western blotting. Caspase-1-like protease activity was determined by a colorimetric tetrapeptide substrate.

Results

The morphology of the retina and the amplitudes of the a and b waves of the ERGs of Casp1–/– mice did not differ from those of WT mice. After the light exposure, TUNEL-positive cells were observed in the outer nuclear layer of the WT mice retina. The number of TUNEL-positive photoreceptor nuclei after the light exposure, and the number of nuclei in the inner nuclear layer after the ischemia–reperfusion injury, were significantly less in Casp1–/– mice than in WT mice. There were more caspase-1-positive photoreceptor cells in WT mice after the light injury. The inner retinal layer of Casp1–/– mice was significantly thicker in Casp1–/– mice than in WT mice 2 weeks after the ischemic insult.

Conclusions

Retinal neuronal apoptosis was less prominent in Casp1–/– mice after excessive light exposure and ischemia–reperfusion injury. These data indicate that caspase-1 plays a role in retinal neuronal apoptosis. Jpn J Ophthalmol 2006;50:417–425 © Japanese Ophthalmological Society 2006

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

Similar content being viewed by others

References

  1. RW Nickells DJ Zack (1996) ArticleTitleApoptosis in ocular disease: a molecular overview Ophthalmic Genet 17 145–165 Occurrence Handle1:STN:280:DyaK2s7msVWnsQ%3D%3D Occurrence Handle10.3109/13816819609057889 Occurrence Handle9010866

    Article  CAS  PubMed  Google Scholar 

  2. PS Rosenbaum H Gupta SI Savitz DM Rosenbaum (1997) ArticleTitleApoptosis in the retina Clin Neurosci 4 224–232 Occurrence Handle1:STN:280:DyaK2svjslOitw%3D%3D Occurrence Handle9292248

    CAS  PubMed  Google Scholar 

  3. LA Levin CL Schlamp RL Spieldoch KM Geszvain RW Nickells (1997) ArticleTitleIdentification of the bcl-2 family of genes in the rat retina Invest Ophthalmol Vis Sci 38 2545–2553 Occurrence Handle1:STN:280:DyaK1c%2Fktlajuw%3D%3D Occurrence Handle9375574

    CAS  PubMed  Google Scholar 

  4. JL Dunaief T Dentchev GS Ying AH Milam (2002) ArticleTitleThe role of apoptosis in age-related macular degeneration Arch Ophthalmol 120 14351442 Occurrence Handle10.1001/archopht.120.11.1435

    Article  Google Scholar 

  5. J Yuan S Shaham S Ledoux HM Ellis HR Horvitz (1993) ArticleTitleThe C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme Cell 75 641–652 Occurrence Handle1:CAS:528:DyaK2cXhsFGhsL0%3D Occurrence Handle10.1016/0092-8674(93)90485-9 Occurrence Handle8242740

    Article  CAS  PubMed  Google Scholar 

  6. P Ramage D Cheneval M Chvei et al. (1995) ArticleTitleExpression, refolding, and autocatalytic proteolytic processing of the interleukin-1 beta-converting enzyme precursor J Biol Chem 270 9378–9383 Occurrence Handle1:CAS:528:DyaK2MXlt1ajtLs%3D Occurrence Handle10.1074/jbc.270.16.9378 Occurrence Handle7721861

    Article  CAS  PubMed  Google Scholar 

  7. NA Thornberry TA Rano EP Peterson et al. (1997) ArticleTitleA combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis J Biol Chem 272 17907–17911 Occurrence Handle1:CAS:528:DyaK2sXkslKgtbc%3D Occurrence Handle10.1074/jbc.272.29.17907 Occurrence Handle9218414

    Article  CAS  PubMed  Google Scholar 

  8. DW Nicholson (1999) ArticleTitleCaspase structure, proteolytic substrates, and function during apoptotic cell death Cell Death Differ 6 1028–1042 Occurrence Handle1:CAS:528:DC%2BD3cXivVeqsQ%3D%3D Occurrence Handle10.1038/sj.cdd.4400598 Occurrence Handle10578171

    Article  CAS  PubMed  Google Scholar 

  9. S Shahinfar DP Edward MO Tso (1991) ArticleTitleA pathologic study of photo-receptor cell death in retinal photic injury Curr Eye Res 10 47–59 Occurrence Handle1:STN:280:DyaK3M3jtVyltQ%3D%3D Occurrence Handle10.3109/02713689109007610 Occurrence Handle2029848

    Article  CAS  PubMed  Google Scholar 

  10. AS Abler CJ Chang J Ful MO Tso TT Lam (1996) ArticleTitlePhotic injury triggers apoptosis of photoreceptor cells Res Commun Mol Pathol Pharmacol 92 177–189 Occurrence Handle1:CAS:528:DyaK28Xjtlyltrc%3D Occurrence Handle8774071

    CAS  PubMed  Google Scholar 

  11. F Hafezi A Marti C Grimm A Wenzel CE Reme (1999) ArticleTitleDifferential DNA binding activities of the transcription factors AP-1 and Oct-1 during light-induced apoptosis of photoreceptors Vision Res 39 2511–2518 Occurrence Handle1:CAS:528:DyaK1MXjtFyqtbY%3D Occurrence Handle10.1016/S0042-6989(98)00313-7 Occurrence Handle10396620

    Article  CAS  PubMed  Google Scholar 

  12. F Hafezi JP Steinbach A Marti et al. (1997) ArticleTitleThe absence of c-fos prevents light-induced apoptotic cell death of photoreceptors in retinal degeneration in vivo Nat Med 3 346–349 Occurrence Handle1:CAS:528:DyaK2sXhsFGqsbw%3D Occurrence Handle10.1038/nm0397-346 Occurrence Handle9055866

    Article  CAS  PubMed  Google Scholar 

  13. J Chen JG Flannery MM LaVail et al. (1996) ArticleTitleBcl-2 overexpression reduces apoptotic photoreceptor cell death in three different retinal degenerations Proc Natl Acad Sci U S A 93 7042–7047 Occurrence Handle1:CAS:528:DyaK28Xkt1Whtr0%3D Occurrence Handle10.1073/pnas.93.14.7042 Occurrence Handle8692941 Occurrence Handle38932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. RM Joseph T Li (1996) ArticleTitleOverexpression of Bcl-2 or Bcl-XL transgenes and photoreceptor degeneration Invest Ophthalmol Vis Sci 37 2434–2446 Occurrence Handle1:STN:280:DyaK2s%2Foslyhsw%3D%3D Occurrence Handle8933760

    CAS  PubMed  Google Scholar 

  15. RJ Carmody AJ McGowan TG Cotter (1999) ArticleTitleReactive oxygen species as mediators of photoreceptor apoptosis in vitro Exp Cell Res 248 520–530 Occurrence Handle1:CAS:528:DyaK1MXis1Klu74%3D Occurrence Handle10.1006/excr.1998.4421 Occurrence Handle10222143

    Article  CAS  PubMed  Google Scholar 

  16. RR Krishnamoorthy MJ Crawford MM Chaturvedi et al. (1999) ArticleTitlePhoto-oxidative stress down-modulates the activity of nuclear factor-kappaB via involvement of caspase-1, leading to apoptosis of photoreceptor cells J Biol Chem 274 3734–3743 Occurrence Handle1:CAS:528:DyaK1MXhtVemt7s%3D Occurrence Handle10.1074/jbc.274.6.3734 Occurrence Handle9920926

    Article  CAS  PubMed  Google Scholar 

  17. C Grimm A Wenzel F Hafezi CE Reme (2000) ArticleTitleGene expression in the mouse retina: the effect of damaging light Mol Vis 6 252–260 Occurrence Handle1:CAS:528:DC%2BD3MXhtl2rtrc%3D Occurrence Handle11134582

    CAS  PubMed  Google Scholar 

  18. T Wu SK Chiang FY Chau MO Tso (2003) ArticleTitleLight-induced photoreceptor degeneration may involve the NF kappa B/caspase-1 pathway in vivo Brain Res 967 19–26 Occurrence Handle1:CAS:528:DC%2BD3sXitV2gsLs%3D Occurrence Handle10.1016/S0006-8993(02)04125-2 Occurrence Handle12650962

    Article  CAS  PubMed  Google Scholar 

  19. M Donovan RJ Carmody TG Cotter (2001) ArticleTitleLight-induced photoreceptor apoptosis in vivo requires neuronal nitric-oxide synthase and guanylate cyclase activity and is caspase-3-independent J Biol Chem 276 23000–23008 Occurrence Handle1:CAS:528:DC%2BD3MXkvVamuro%3D Occurrence Handle10.1074/jbc.M005359200 Occurrence Handle11278285

    Article  CAS  PubMed  Google Scholar 

  20. S Kuroiwa N Katai H Shibuki et al. (1998) ArticleTitleExpression of cell cycle-related genes in dying cells in retinal ischemic injury Invest Ophthalmol Vis Sci 39 610–617 Occurrence Handle1:STN:280:DyaK1c7mt1Gitw%3D%3D Occurrence Handle9501873

    CAS  PubMed  Google Scholar 

  21. H Shibuki N Katai S Kuroiwa et al. (1998) ArticleTitleProtective effect of adult T-cell leukemia-derived factor on retinal ischemia-reperfusion injury in the rat Invest Ophthalmol Vis Sci 39 1470–1477 Occurrence Handle1:STN:280:DyaK1czitF2gsQ%3D%3D Occurrence Handle9660496

    CAS  PubMed  Google Scholar 

  22. N Katai N Yoshimura (1999) ArticleTitleApoptotic retinal neuronal death by ischemia-reperfusion is executed by two distinct caspase family proteases Invest Ophthalmol Vis Sci 40 2697–2705 Occurrence Handle1:STN:280:DyaK1MvjsleltQ%3D%3D Occurrence Handle10509668

    CAS  PubMed  Google Scholar 

  23. T Kurokawa N Katai H Shibuki et al. (1999) ArticleTitleBDNF diminishes caspase-2 but not c-Jun immunoreactivity of neurons in retinal ganglion cell layer after transient ischemia Invest Ophthalmol Vis Sci 40 3006–3011 Occurrence Handle1:STN:280:DC%2BD3c%2FhsFymtQ%3D%3D Occurrence Handle10549664

    CAS  PubMed  Google Scholar 

  24. H Shibuki N Katai J Yodoi K Uchida N Yoshimura (2000) ArticleTitleLipid peroxidation and peroxynitrite in retinal ischemia–reperfusion injury Invest Ophthalmol Vis Sci 41 3607–3614 Occurrence Handle1:STN:280:DC%2BD3cvot1ymtw%3D%3D Occurrence Handle11006259

    CAS  PubMed  Google Scholar 

  25. M Singh SI Savitz R Hoque et al. (2001) ArticleTitleCell-specific caspase expression by different neuronal phenotypes in transient retinal ischemia J Neurochem 77 466–475 Occurrence Handle1:CAS:528:DC%2BD3MXjtVOlu7w%3D Occurrence Handle10.1046/j.1471-4159.2001.00258.x Occurrence Handle11299309

    Article  CAS  PubMed  Google Scholar 

  26. TT Lam AS Abler MOM Tso (1999) ArticleTitleApoptosis and caspases after ischemia–reperfusion injury in rat retina Invest Ophthalmol Vis Sci 40 967–975 Occurrence Handle1:STN:280:DyaK1M3gtVCitQ%3D%3D Occurrence Handle10102294

    CAS  PubMed  Google Scholar 

  27. C Zhang DM Rosenbaum AR Shaikh et al. (2002) ArticleTitleIschemic preconditioning attenuates apoptotic cell death in the rat retina Invest Ophthalmol Vis Sci 43 3059–3066 Occurrence Handle12202530

    PubMed  Google Scholar 

  28. K Kuida JA Lippke G Ku et al. (1995) ArticleTitleAltered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme Science 267 2000–2003 Occurrence Handle1:CAS:528:DyaK2MXkslOkurw%3D Occurrence Handle10.1126/science.7535475 Occurrence Handle7535475

    Article  CAS  PubMed  Google Scholar 

  29. Y Gu K Kuida H Tsutsui et al. (1997) ArticleTitleActivation of interferon-gamma inducing factor mediated by interleukin-1beta converting enzyme Science 275 206–209 Occurrence Handle1:CAS:528:DyaK2sXksFyrsQ%3D%3D Occurrence Handle10.1126/science.275.5297.206 Occurrence Handle8999548

    Article  CAS  PubMed  Google Scholar 

  30. P Li H Allen S Banerjee et al. (1995) ArticleTitleMice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock Cell 80 401–411 Occurrence Handle1:CAS:528:DyaK2MXjslWkt7k%3D Occurrence Handle10.1016/0092-8674(95)90490-5 Occurrence Handle7859282

    Article  CAS  PubMed  Google Scholar 

  31. DM Rosenbaum PS Rosenbaum H Gupta et al. (1998) ArticleTitleThe role of the p53 protein in the selective vulnerability of the inner retina to transient ischemia Invest Ophthalmol Vis Sci 39 2132–2139 Occurrence Handle1:STN:280:DyaK1cvjt1CgtA%3D%3D Occurrence Handle9761292

    CAS  PubMed  Google Scholar 

  32. Y Gavrieli Y Sherman SA Ben-Sasson (1992) ArticleTitleIdentification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation J Cell Biol 119 493–501 Occurrence Handle1:CAS:528:DyaK38XmtVyhsbs%3D Occurrence Handle10.1083/jcb.119.3.493 Occurrence Handle1400587

    Article  CAS  PubMed  Google Scholar 

  33. MM Bradford (1976) ArticleTitleA rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding Anal Biochem 72 248–254 Occurrence Handle1:CAS:528:DyaE28XksVehtrY%3D Occurrence Handle10.1016/0003-2697(76)90527-3 Occurrence Handle942051

    Article  CAS  PubMed  Google Scholar 

  34. CK Joo JS Choi HW Ko et al. (1999) ArticleTitleNecrosis and apoptosis after retinal ischemia: involvement of NMDA-mediated excitotoxicity and p53 Invest Ophthalmol Vis Sci 40 713–720 Occurrence Handle1:STN:280:DyaK1M7msFaqug%3D%3D Occurrence Handle10067975

    CAS  PubMed  Google Scholar 

  35. RA Black SR Krohnheim M Cantrell et al. (1988) ArticleTitleGeneration of biologically active interleukin-1 beta by proteolytic cleavage of the inactive precursor J Biol Chem 263 9437–9442 Occurrence Handle1:CAS:528:DyaL1cXksFaqt7w%3D Occurrence Handle3288634

    CAS  PubMed  Google Scholar 

  36. C Bossenmeyer-Pourie V Koziel JL Daval (2000) ArticleTitleInvolvement of caspase-1 proteases in hypoxic brain injury. Effects of their inhibitors in developing neurons Neuroscience 95 1157–1165 Occurrence Handle1:CAS:528:DC%2BD3cXhtFWqtb0%3D Occurrence Handle10.1016/S0306-4522(99)00501-1 Occurrence Handle10682722

    Article  CAS  PubMed  Google Scholar 

  37. H Hara K Fink M Endres et al. (1997) ArticleTitleAttenuation of transient focal cerebral ischemic injury in transgenic mice expressing a mutant ICE inhibitory protein J Cereb Blood Flow Metab 17 370 Occurrence Handle1:CAS:528:DyaK2sXjt1Gktrs%3D Occurrence Handle10.1097/00004647-199704000-00002 Occurrence Handle9143219

    Article  CAS  PubMed  Google Scholar 

  38. RM Friedlander V Gagliardini H Hara et al. (1997) ArticleTitleExpression of a dominant negative mutant of interleukin-1 beta converting enzyme in transgenic mice prevents neuronal cell death induced by trophic factor withdrawal and ischemic brain injury J Exp Med 185 933–940 Occurrence Handle1:CAS:528:DyaK2sXhsFKnsbg%3D Occurrence Handle10.1084/jem.185.5.933 Occurrence Handle9120399 Occurrence Handle2196165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. C Eriksson R Tehranian K Iverfeldt B Winblad M Schultzberg (2000) ArticleTitleIncreased expression of mRNA encoding interleukin-1beta and caspase-1, and the secreted isoform of interleukin-1 receptor antagonist in the rat brain following systemic kainic acid administration J Neurosci Res 60 266–279 Occurrence Handle1:CAS:528:DC%2BD3cXisVWjur0%3D Occurrence Handle10.1002/(SICI)1097-4547(20000415)60:2<266::AID-JNR16>3.0.CO;2-P Occurrence Handle10740232

    Article  CAS  PubMed  Google Scholar 

  40. H Hara RM Friedlander V Gagliardini et al. (1997) ArticleTitleInhibition of interleukin 1 beta converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage Proc Natl Acad Sci U S A 94 2007–2012 Occurrence Handle1:CAS:528:DyaK2sXhslersbg%3D Occurrence Handle10.1073/pnas.94.5.2007 Occurrence Handle9050895 Occurrence Handle20033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. A Benchoua C Guegan C Couriaud et al. (2001) ArticleTitleSpecific caspase pathways are activated in the two stages of cerebral infarction J Neurosci 21 7127–7134 Occurrence Handle1:CAS:528:DC%2BD3MXmvFWhtbk%3D Occurrence Handle11549723

    CAS  PubMed  Google Scholar 

  42. M Hangai N Yoshimura M Yoshida K Yabuuchi Y Honda (1995) ArticleTitleInterleukin-1 gene expression in transient retinal ischemia in the rat Invest Ophthalmol Vis Sci 36 571–578 Occurrence Handle1:STN:280:DyaK2M7pslelsg%3D%3D Occurrence Handle7890488

    CAS  PubMed  Google Scholar 

  43. S Yoneda H Tanihara N Kido et al. (2001) ArticleTitleInterleukin-1 beta mediates ischemic injury in the rat retina Exp Eye Res 73 661–667 Occurrence Handle1:CAS:528:DC%2BD3MXptFWrtb4%3D Occurrence Handle10.1006/exer.2001.1072 Occurrence Handle11747366

    Article  CAS  PubMed  Google Scholar 

  44. XH Liu D Kwon GP Schielke et al. (1999) ArticleTitleMice deficient in interleukin-1 converting enzyme are resistant to neonatal hypoxic-ischemic brain damage J Cereb Blood Flow Metab 19 1099–1108 Occurrence Handle1:CAS:528:DC%2BD3cXks1SntLY%3D Occurrence Handle10.1097/00004647-199910000-00006 Occurrence Handle10532634

    Article  CAS  PubMed  Google Scholar 

  45. GP Schielke GY Yang BD Shivers AL Betz (1998) ArticleTitleReduced ischemic brain injury in interleukin-1β converting enzyme-deficient mice J Cereb Blood Flow Metab 18 180–185 Occurrence Handle1:CAS:528:DyaK1cXhtFWjsrg%3D Occurrence Handle10.1097/00004647-199802000-00009 Occurrence Handle9469161

    Article  CAS  PubMed  Google Scholar 

  46. TG Gorgels D Van Norren (1998) ArticleTitleTwo spectral types of retinal light damage occur in albino as well as in pigmented rat: no essential role for melanin Exp Eye Res 66 155–162 Occurrence Handle1:CAS:528:DyaK1cXht12iuro%3D Occurrence Handle10.1006/exer.1997.0416 Occurrence Handle9533842

    Article  CAS  PubMed  Google Scholar 

  47. MM LaVail GM Gorrin (1987) ArticleTitleProtection from light damage by ocular pigmentation: analysis using experimental chimeras and translocation mice Exp Eye Res 44 877–889 Occurrence Handle1:STN:280:DyaL1c%2FgsVymsQ%3D%3D Occurrence Handle10.1016/S0014-4835(87)80050-7 Occurrence Handle3653278

    Article  CAS  PubMed  Google Scholar 

  48. MM LaVail GM Gorrin MA Repaci D Yasumura (1987) ArticleTitleLight-induced retinal degeneration in albino mice and rats: strain and species differences Prog Clin Biol Res 247 439–454 Occurrence Handle1:STN:280:DyaL1c%2FmvVOmsA%3D%3D Occurrence Handle3685038

    CAS  PubMed  Google Scholar 

  49. M Hangai N Yoshimura Y Honda (1996) ArticleTitleIncreased cytokine gene expression in rat retina following transient ischemia Ophthalmic Res 28 248–254 Occurrence Handle1:CAS:528:DyaK28XmtF2ksrk%3D Occurrence Handle10.1159/000267910 Occurrence Handle8878188

    Article  CAS  PubMed  Google Scholar 

  50. RN Sanchez CK Chan S Garg et al. (2003) ArticleTitleInterleukin-6 in retinal ischemia reperfusion injury in rats Invest Ophthalmol Vis Sci 44 4006–4011 Occurrence Handle10.1167/iovs.03-0040 Occurrence Handle12939322

    Article  PubMed  Google Scholar 

  51. Y Zhou LE Lindner GC Chiou KP Morgan Z Li (2000) ArticleTitleTransient retinal ischemia–reperfusion in rats Chin Med J 113 461–465 Occurrence Handle1:CAS:528:DC%2BD3cXktVygs7w%3D Occurrence Handle11776107

    CAS  PubMed  Google Scholar 

  52. V Fontaine S Mohand-Said N Hanoteau et al. (2002) ArticleTitleNeurodegenerative and neuroprotective effects of tumor necrosis factor (TNF) in retinal ischemia: opposite roles of TNF receptor 1 and TNF receptor 2 J Neurosci 22 RC216 Occurrence Handle11917000

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Ophthalmology, Shinshu University School of Medicine, Matsumoto, Japan

    Jun Arai & Naomichi Katai

  2. Vertex Pharmaceuticals Incorporated, Cambridge, Massachusetts, USA

    Keisuke Kuida

  3. Research Support Center for Human and Environmental Sciences, Shinshu University, Matsumoto, Japan

    Takanobu Kikuchi

  4. Department of Ophthalmology and Visual Sciences, Kyoto University Graduate School of Medicine, Kyoto, Japan

    Nagahisa Yoshimura

Authors
  1. Jun Arai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Naomichi Katai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Keisuke Kuida
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takanobu Kikuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nagahisa Yoshimura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Naomichi Katai.

About this article

Cite this article

Arai, J., Katai, N., Kuida, K. et al. Decreased Retinal Neuronal Cell Death in Caspase-1 Knockout Mice. Jpn J Ophthalmol 50, 417–425 (2006). https://doi.org/10.1007/s10384-006-0352-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10384-006-0352-y

Key words

Search

Navigation