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Oxidative Medicine and Cellular Longevity
Volume 2015, Article ID 787561, 15 pages
http://dx.doi.org/10.1155/2015/787561
Research Article

Pituitary Adenylate Cyclase-Activating Polypeptide Reverses Ammonium Metavanadate-Induced Airway Hyperresponsiveness in Rats

1Laboratory of Integrated Physiology, Science Faculty of Bizerte, Carthage University, 7021 Zarzouna, Tunisia
2National Institute of Health and Medical Research (INSERM), U982, 76821 Mont-Saint-Aignan Cedex, France
3Institute for Research and Innovation in Biomedicine (IRIB), Normandy University, 76821 Mont-Saint-Aignan Cedex, France
4Laboratory of Neuronal and Neuroendocrine Differentiation and Communication, Rouen University, 76821 Mont-Saint-Aignan Cedex, France
5Laboratory of Physiology and Functional Exploration, CHU Farhat Hached, 4000 Sousse, Tunisia
6Laboratory of Pathologic Anatomy, CHU Farhat Hached, 4000 Sousse, Tunisia

Received 8 December 2014; Revised 15 May 2015; Accepted 18 May 2015

Academic Editor: Vladimir Jakovljevic

Copyright © 2015 Mounira Tlili et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. G. Barceloux, “Vanadium,” Journal of Toxicology: Clinical Toxicology, vol. 37, no. 2, pp. 265–278, 1999. View at Google Scholar
  2. M. A. Woodin, Y. Liu, D. Neuberg, R. Hauser, T. J. Smith, and D. C. Christiani, “Acute respiratory symptoms in workers exposed to vanadium-rich fuel-oil ash,” The American Journal of Industrial Medicine, vol. 37, no. 4, pp. 353–363, 2000. View at Publisher · View at Google Scholar · View at Scopus
  3. R. A. Nayler and M. P. Sparrow, “Mechanism of vanadate-induced contraction of airways smooth muscle of the guinea-pig,” British Journal of Pharmacology, vol. 80, no. 1, pp. 163–172, 1983. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Cortijo, V. Villagrasa, M. Martí-Cabrera et al., “The spasmogenic effects of vanadate in human isolated bronchus,” British Journal of Pharmacology, vol. 121, no. 7, pp. 1339–1349, 1997. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Ding, J. J. Li, S. S. Leonard et al., “Vanadate-induced activation of activator protein-1: role of reactive oxygen species,” Carcinogenesis, vol. 20, no. 4, pp. 663–668, 1999. View at Publisher · View at Google Scholar · View at Scopus
  6. L. M. Pierce, F. Alessandrini, J. J. Godleski, and J. D. Paulauskis, “Vanadium-induced chemokine mRNA expression and pulmonary inflammation,” Toxicology and Applied Pharmacology, vol. 138, no. 1, pp. 1–11, 1996. View at Publisher · View at Google Scholar · View at Scopus
  7. M. D. Cohen, Z. Yang, J. T. Zelikoff, and R. B. Schlesinger, “Pulmonary immunotoxicity of inhaled ammonium metavanadate in fisher 344 rats,” Fundamental and Applied Toxicology, vol. 33, no. 2, pp. 254–263, 1996. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Z. Byczkowski and A. P. Kulkarni, “Vanadium redox cycling, lipid peroxidation and co-oxygenation of benzo(a)pyrene-7,8-dihydrodiol,” Biochimica et Biophysica Acta—Lipids and Lipid Metabolism, vol. 1125, no. 2, pp. 134–141, 1992. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Miyata, A. Arimura, R. R. Dahl et al., “Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells,” Biochemical and Biophysical Research Communications, vol. 164, no. 1, pp. 567–574, 1989. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Lindén, L.-O. Cardell, S. Yoshihara, and J. A. Nadel, “Bronchodilation by pituitary adenylate cyclase-activating peptide and related peptides,” European Respiratory Journal, vol. 14, no. 2, pp. 443–451, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Kinhult, J. A. Andersson, R. Uddman, P. Stjärne, and L.-O. Cardell, “Pituitary adenylate cyclase-activating peptide 38 a potent endogenously produced dilator of human airways,” European Respiratory Journal, vol. 15, no. 2, pp. 243–247, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. R. J. A. Wilson and K. J. Cummings, “Pituitary adenylate cyclase-activating polypeptide is vital for neonatal survival and the neuronal control of breathing,” Respiratory Physiology & Neurobiology, vol. 164, no. 1-2, pp. 168–178, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Aizawa, M. Shigyo, K. Matsumoto, H. Inoue, H. Koto, and N. Hara, “PACAP reverses airway hyperresponsiveness induced by Ozone exposure in Guinea pigs,” Respiration, vol. 66, no. 6, pp. 538–542, 1999. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Delgado, E. J. Munoz-Elias, Y. Kan et al., “Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit tumor necrosis factor α transcriptional activation by regulating nuclear factor-κB and cAMP response element-binding protein/c-Jun,” The Journal of Biological Chemistry, vol. 273, no. 47, pp. 31427–31436, 1998. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Delgado, D. Pozo, C. Martinez et al., “Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit endotoxin-induced TNF-α production by macrophages: in vitro and in vivo studies,” Journal of Immunology, vol. 162, no. 4, pp. 2358–2367, 1999. View at Google Scholar · View at Scopus
  16. M. Delgado and D. Ganea, “Vasoactive intestinal peptide and pituitary adenylate cyclase activating polypeptide inhibit the MEKK1/MEK4/JNK signaling pathway in LPS-stimulated macrophages,” Journal of Neuroimmunology, vol. 110, no. 1-2, pp. 97–105, 2000. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Martinez, M. Delgado, D. Pozo et al., “VIP and PACAP enhance IL-6 release and mRNA levels in resting peritoneal macrophages: in vitro and in vivo studies,” Journal of Neuroimmunology, vol. 85, no. 2, pp. 155–167, 1998. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Martínez, M. Delgado, D. Pozo et al., “Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide modulate endotoxin-induced IL-6 production by murine peritoneal macrophages,” Journal of Leukocyte Biology, vol. 63, no. 5, pp. 591–601, 1998. View at Google Scholar · View at Scopus
  19. M. Delgado, E. J. Munoz-Elias, R. P. Gomariz, and D. Ganea, “Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide prevent inducible nitric oxide synthase transcription in macrophages by inhibiting NF-kB and IFN regulatory factor 1 activation,” The Journal of Immunology, vol. 162, no. 8, pp. 4685–4696, 1999. View at Google Scholar · View at Scopus
  20. M. Takaya and K. Sawatari, “Speciation of vanadium(IV) and vanadium(V) using ion-exchange chromatography and ICP-AES,” Industrial Health, vol. 32, no. 3, pp. 165–178, 1994. View at Publisher · View at Google Scholar · View at Scopus
  21. E. F. Hartree, “Determination of protein: a modification of the lowry method that gives a linear photometric response,” Analytical Biochemistry, vol. 48, no. 2, pp. 422–427, 1972. View at Publisher · View at Google Scholar · View at Scopus
  22. H. H. Draper and M. Hadley, “Malondialdehyde determination as index of lipid peroxidation,” Methods in Enzymology, vol. 186, pp. 421–431, 1990. View at Publisher · View at Google Scholar · View at Scopus
  23. F. Tietze, “Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues,” Analytical Biochemistry, vol. 27, no. 3, pp. 502–522, 1969. View at Publisher · View at Google Scholar · View at Scopus
  24. H. Aebi, “Catalase in vitro,” Methods in Enzymology, vol. 105, no. 1, pp. 121–126, 1984. View at Publisher · View at Google Scholar · View at Scopus
  25. W. Nakamura, S. Hosoda, and K. Hayashi, “Purification and properties of rat liver glutathione peroxidase,” Biochimica et Biophysica Acta, vol. 358, no. 2, pp. 251–261, 1974. View at Publisher · View at Google Scholar · View at Scopus
  26. H. P. Misra and I. Fridovich, “The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase,” The Journal of Biological Chemistry, vol. 247, no. 10, pp. 3170–3175, 1972. View at Google Scholar · View at Scopus
  27. L. C. Green, D. A. Wagner, J. Glogowski, P. L. Skipper, J. S. Wishnok, and S. R. Tannenbaum, “Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids,” Analytical Biochemistry, vol. 126, no. 1, pp. 131–138, 1982. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Kakinuma, T. Yamaguchi, and M. Kaneda, “A determination of H2O2 release by the treatment of human blood polymorphonuclear leukocytes with myristate,” Journal of Biochemistry, vol. 86, no. 1, pp. 87–95, 1979. View at Google Scholar · View at Scopus
  29. A. L. James, J. G. Elliot, R. L. Jones et al., “Airway smooth muscle hypertrophy and hyperplasia in asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 185, no. 10, pp. 1058–1064, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Sapienza, T. Du, D. H. Eidelman, N. S. Wang, and J. G. Martin, “Structural changes in the airways of sensitized Brown Norway rats after antigen challenge,” American Review of Respiratory Disease, vol. 144, no. 2, pp. 423–427, 1991. View at Publisher · View at Google Scholar · View at Scopus
  31. Agency for Toxic Substances and Disease Registry (ATSDR), Toxicalogical Profile for Vanadium, Agency for Toxic Substances and Disease Registry, US Department of Health and Human Services, Atlanta, Ga, USA, 2012.
  32. B. V. Venkataraman and S. Sudha, “Vanadium toxicity,” Asian Journal of Experimental Sciences, vol. 19, pp. 127–134, 2005. View at Google Scholar
  33. D. C. Crans, M. Mahroof-Tahir, and A. D. Keramidas, “Vanadium chemistry and biochemistry of relevance for use of vanadium compounds as antidiabetic agents,” Molecular and Cellular Biochemistry, vol. 153, no. 1-2, pp. 17–24, 1995. View at Publisher · View at Google Scholar · View at Scopus
  34. M. D. Cohen, M. Sisco, C. Prophete et al., “Pulmonary immunotoxic potentials of metals are governed by select physicochemical properties: vanadium agents,” Journal of Immunotoxicology, vol. 4, no. 1, pp. 49–60, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. M. D. Cohen, Z. Yang, J. T. Zelikoff, and R. B. Schlesinger, “Pulmonary immunotoxicity of inhaled ammonium metavanadate in Fisher 344 rats,” Fundamental and Applied Toxicology, vol. 33, no. 2, pp. 254–263, 1996. View at Publisher · View at Google Scholar · View at Scopus
  36. H. Imura, A. Shimada, M. Naota et al., “Vanadium toxicity in mice: possible impairment of lipid metabolism and mucosal epithelial cell necrosis in the small intestine,” Toxicologic Pathology, vol. 41, no. 6, pp. 842–856, 2013. View at Publisher · View at Google Scholar
  37. J. Edel and E. Sabbioni, “Retention of intratracheally instilled and ingested tetravalent and pentavalent vanadium in the rat,” Journal of Trace Elements and Electrolytes in Health and Disease, vol. 2, no. 1, pp. 23–30, 1988. View at Google Scholar · View at Scopus
  38. M. D. Cohen, S. Becker, R. Devlin, R. B. Schlesinger, and J. T. Zelikoff, “Effects of vanadium upon polyi:C-induced responses in rat lung and alveolar macrophages,” Journal of Toxicology and Environmental Health, vol. 51, no. 6, pp. 591–608, 1997. View at Publisher · View at Google Scholar · View at Scopus
  39. M. D. Cohen, M. Sisco, C. Prophete et al., “Effects of metal compounds with distinct physicochemical properties on iron homeostasis and antibacterial activity in the lungs: chromium and vanadium,” Inhalation Toxicology, vol. 22, no. 2, pp. 169–178, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. E. A. Knecht, W. J. Moorman, J. C. Clark, D. W. Lynch, and T. R. Lewis, “Pulmonary effects of acute vanadium pentoxide inhalation in monkeys,” American Review of Respiratory Disease, vol. 132, no. 6, pp. 1181–1185, 1985. View at Google Scholar · View at Scopus
  41. M. D. Cohen and C. I. Wei, “Effects of ammonium metavanadate treatment upon macrophage glutathione redox cycle activity, superoxide production, and intracellular glutathione status,” Journal of Leukocyte Biology, vol. 44, no. 2, pp. 122–129, 1988. View at Google Scholar · View at Scopus
  42. M. D. Cohen, C. I. Wei, H. Tan, and K. J. Kao, “Effect of ammonium metavanadate on the murine immune response,” Journal of Toxicology and Environmental Health, vol. 19, no. 2, pp. 279–298, 1986. View at Publisher · View at Google Scholar · View at Scopus
  43. A. M. Cortizo, L. Bruzzone, S. Molinuevo, and S. B. Etcheverry, “A possible role of oxidative stress in the vanadium-induced cytotoxicity in the MC3T3E1 osteoblast and UMR106 osteosarcoma cell lines,” Toxicology, vol. 147, no. 2, pp. 89–99, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. B. Mukherjee, B. Patra, S. Mahapatra, P. Banerjee, A. Tiwari, and M. Chatterjee, “Vanadium—an element of atypical biological significance,” Toxicology Letters, vol. 150, no. 2, pp. 135–143, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. E. Sabbioni, L. Clerici, and A. Brazzelli, “Different effects of vanadium ions on some DNA metabolizing enzymes,” Journal of Toxicology and Environmental Health, vol. 12, no. 4–6, pp. 737–748, 1983. View at Publisher · View at Google Scholar · View at Scopus
  46. E. Sabbioni, G. Pozzi, S. Devos, A. Pintar, L. Casella, and M. Fischbach, “The intensity of vanadium(V)-induced cytotoxicity and morphological transformation in BALB/3T3 cells is dependent on glutathione-mediated bioreduction to vanadium(IV),” Carcinogenesis, vol. 14, no. 12, pp. 2565–2568, 1993. View at Google Scholar · View at Scopus
  47. M. Á. Serra, A. Pintar, L. Casella, and E. Sabbioni, “Vanadium effect on the activity of horseradish peroxidase, catalase, glutathione peroxidase, and superoxide dismutase in vitro,” Journal of Inorganic Biochemistry, vol. 46, no. 3, pp. 161–174, 1992. View at Publisher · View at Google Scholar · View at Scopus
  48. L. O. Cardell, R. Uddman, A. Luts, and F. Sundler, “Pituitary adenylate cyclase activating peptide (PACAP) in guinea-pig lung: distribution and dilatory effects,” Regulatory Peptides, vol. 36, no. 3, pp. 379–390, 1991. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Linden, S. Yoshihara, B. Chan, and J. A. Nadel, “Inhibition of bronchoconstriction by pituitary adenylate cyclase activating polypeptide (PACAP 1-27) in guinea-pigs in vivo,” British Journal of Pharmacology, vol. 115, no. 6, pp. 913–916, 1995. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Lindén, L.-O. Cardell, S. Yoshihara, P. Stjärne, and J. A. Nadel, “PACAP 1–38 as an inhaled bronchodilator in guinea pigs in vivo,” Peptides, vol. 19, no. 1, pp. 93–98, 1998. View at Publisher · View at Google Scholar · View at Scopus
  51. B. R. Nechay, L. B. Nanninga, and P. S. E. Nechay, “Vanadyl (IV) and vanadate (V) binding to selected endogenous phosphate, carboxyl, and amino ligands; calculations of cellular vanadium species distribution,” Archives of Biochemistry and Biophysics, vol. 251, no. 1, pp. 128–138, 1986. View at Publisher · View at Google Scholar · View at Scopus
  52. B. R. Nechay, “Mechanisms of action of vanadium,” Annual Review of Pharmacology and Toxicology, vol. 24, no. 1, pp. 501–524, 1984. View at Publisher · View at Google Scholar
  53. L. Wang, D. Medan, R. Mercer et al., “Vanadium-induced apoptosis and pulmonary inflammation in mice: role of reactive oxygen species,” Journal of Cellular Physiology, vol. 195, no. 1, pp. 99–107, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. S. S. Soares, H. Martins, C. Gutiérrez-Merino, and M. Aureliano, “Vanadium and cadmium in vivo effects in teleost cardiac muscle: metal accumulation and oxidative stress markers,” Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, vol. 147, no. 2, pp. 168–178, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. M. P. Bindu and P. T. Annamalai, “Combined effect of alcohol and cigarette smoke on lipid peroxidation and antioxidant status in rats,” Indian Journal of Biochemistry & Biophysics, vol. 41, no. 1, pp. 40–44, 2004. View at Google Scholar · View at Scopus
  56. T. Toya, K. Fukuda, M. Takaya, and H. I. Arito, “Lung lesions induced by intratracheal instillation of vanadium pentoxide powder in rats,” Industrial Health, vol. 39, no. 1, pp. 8–15, 2001. View at Publisher · View at Google Scholar · View at Scopus
  57. Z. Zhang, C. S. Huang, J. X. Li et al., “Vanadate-induced cell growth regulation and the role of reactive oxygen species,” Archives of Biochemistry and Biophysics, vol. 392, no. 2, pp. 311–320, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. G. M. Grabowski, J. D. Paulauskis, and J. J. Godleski, “Mediating phosphorylation events in the vanadium-induced respiratory burst of alveolar macrophages,” Toxicology and Applied Pharmacology, vol. 156, no. 3, pp. 170–178, 1999. View at Publisher · View at Google Scholar · View at Scopus
  59. X. L. Shi and N. S. Dalal, “Vanadate-mediated hydroxyl radical generation from superoxide radical in the presence of NADH: Haber-Weiss vs Fenton mechanism,” Archives of Biochemistry and Biophysics, vol. 307, no. 2, pp. 336–341, 1993. View at Publisher · View at Google Scholar · View at Scopus
  60. M. R. Siddiqui, A. Taha, K. Moorthy, M. E. Hussain, S. F. Basir, and N. Z. Baquer, “Amelioration of altered antioxidant status and membrane linked functions by vanadium and Trigonella in alloxan diabetic rat brains,” Journal of Biosciences, vol. 30, no. 4, pp. 483–490, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Ścibior, D. Gołębiowska, and I. Niedźwiecka, “Magnesium can protect against vanadium-induced lipid peroxidation in the hepatic tissue,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 802734, 11 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Donaldson, R. Hemming, and F. LaBella, “Vanadium exposure enhances lipid peroxidation in the kidney of rats and mice,” Canadian Journal of Physiology and Pharmacology, vol. 63, no. 3, pp. 196–199, 1985. View at Publisher · View at Google Scholar · View at Scopus
  63. I. Mannazzu, E. Guerra, R. Ferretti, D. Pediconi, and F. Fatichenti, “Vanadate and copper induce overlapping oxidative stress responses in the vanadate-tolerant yeast Hansenula polymorpha,” Biochimica et Biophysica Acta—General Subjects, vol. 1475, no. 2, pp. 151–156, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. B. Botia, D. Seyer, A. Ravni et al., “Peroxiredoxin 2 is involved in the neuroprotective effects of PACAP in cultured cerebellar granule neurons,” Journal of Molecular Neuroscience, vol. 36, no. 1–3, pp. 61–72, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. U. Zor, E. Ferber, P. Gergely, K. Szucs, V. Dombradi, and R. Goldman, “Reactive oxygen species mediate phorbol ester-regulated tyrosine phosphorylation and phospholipase A2 activation: potentiation by vanadate,” Biochemical Journal, vol. 295, no. 3, pp. 879–888, 1993. View at Google Scholar · View at Scopus
  66. S. Koncz and E. J. Horváth, “Synergistic action of rutin and orthovanadate on nitric oxide release from mouse macrophage cells,” Acta Physiologica Hungarica, vol. 87, no. 1, pp. 53–66, 2000. View at Publisher · View at Google Scholar · View at Scopus
  67. A. M. Cortizo, M. Caporossi, G. Lettieri, and S. B. Etcheverry, “Vanadate-induced nitric oxide production: role in osteoblast growth and differentiation,” European Journal of Pharmacology, vol. 400, no. 2-3, pp. 279–285, 2000. View at Publisher · View at Google Scholar · View at Scopus
  68. R. Nakaike, H. Shimokawa, M. K. Owada et al., “Vanadate causes synthesis of endothelium-derived NO via pertussis toxin-sensitive G protein in pigs,” American Journal of Physiology: Heart and Circulatory Physiology, vol. 271, no. 1, pp. H296–H302, 1996. View at Google Scholar · View at Scopus
  69. A. D. Milward, R. Riba, B. Patel, N. G. Oberprieler, and K. M. Naseem, “Sodium orthovanadate induced tyrosine phosphorylation of platelet nitric oxide synthase negatively regulates enzyme activity,” Biochimica et Biophysica Acta—General Subjects, vol. 1760, no. 9, pp. 1411–1417, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. I. W. Chong, M. M. Shi, J. A. Love, D. C. Christiani, and J. D. Paulauskis, “Regulation of chemokine mRNA expression in a rat model of vanadium-induced pulmonary inflammation,” Inflammation, vol. 24, no. 6, pp. 505–517, 2000. View at Publisher · View at Google Scholar · View at Scopus
  71. M. Delgado and D. Ganea, “Inhibition of endotoxin-induced macrophage chemokine production by vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide in vitro and in vivo,” Journal of Immunology, vol. 167, no. 2, pp. 966–975, 2001. View at Publisher · View at Google Scholar · View at Scopus
  72. J. Kinhult, R. Uddman, M. Laan, A. Lindén, and L. O. Cardell, “Pituitary adenylate cyclase-activating peptide inhibits neutrophil chemotaxis,” Peptides, vol. 22, no. 12, pp. 2151–2154, 2001. View at Publisher · View at Google Scholar · View at Scopus
  73. E. Garrido, M. Delgado, C. Martínez, R. P. Gomariz, and M. De la Fuente, “Pituitary adenylate cyclase-activating polypeptide (PACAP38) modulates lymphocyte and macrophage functions: stimulation of adherence and opposite effect on mobility,” Neuropeptides, vol. 30, no. 6, pp. 583–595, 1996. View at Publisher · View at Google Scholar · View at Scopus