Cell death and neurodegeneration in the postnatal development of cerebellar vermis in normal and Reeler mice

Annals of Anatomy

Volumn 207, Issue , 2016, Pages 76-90

  Castagna, Claudia ^a   Merighi, Adalberto ^a   Lossi, Laura ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Apoptosis; Autophagy; Cerebellum; Development; Granule cells; Mouse; Ultrastructure

Indexed keywords

REELIN; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; REELIN PROTEIN; SCLEROPROTEIN; SERINE PROTEINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOPHAGY; BRAIN DEVELOPMENT; BRAIN REGION; CELL DEATH; CELL DENSITY; CELL FUNCTION; CEREBELLUM CORTEX; CEREBELLUM VERMIS; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DISEASE ASSOCIATION; GRANULE CELL; MICROSCOPY; MOLECULAR DYNAMICS; MOUSE; NERVE DEGENERATION; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; REELER MOUSE; ULTRASTRUCTURE; ANIMAL; DEGENERATIVE DISEASE; FEMALE; GENETICS; MALE; MOUSE MUTANT; NERVE CELL; PATHOLOGY;

ANIMALS; APOPTOSIS; AUTOPHAGY; CELL ADHESION MOLECULES, NEURONAL; CEREBELLAR VERMIS; EXTRACELLULAR MATRIX PROTEINS; FEMALE; MALE; MICE; MICE, NEUROLOGIC MUTANTS; NERVE TISSUE PROTEINS; NEURODEGENERATIVE DISEASES; NEURONS; SERINE ENDOPEPTIDASES;

EID: 84962536011     PISSN: 09409602     EISSN: 16180402     Source Type: Journal    
DOI: 10.1016/j.aanat.2016.01.010     Document Type: Article

References (78)

1. Altman, J., Programmed cell death: the paths to suicide. Trends Neurol. Sci. 15 (1992), 278–280.
2. Berezniuk, I., Sironi, J., Callaway, M.B., Castro, L.M., Hirata, I.Y., Ferro, E.S., Fricker, L.D., CCP1/Nna1 functions in protein turnover in mouse brain: implications for cell death in Purkinje cell degeneration mice. FASEB J. 24 (2010), 1813–1823.
3. Blatt, G.J., Eisenman, L.M., A qualitative and quantitative light microscopic study of the inferior olivary complex of normal, reeler, and weaver mutant mice. J. Comp. Neurol. 232 (1985), 117–128.
4. Caddy, K.W., Biscoe, T.J., Structural and quantitative studies on the normal C3H and Lurcher mutant mouse. Philos. Trans. R. Soc. Lond. B. 287 (1979), 167–201.
5. Campbell, D.B., Hess, E.J., Chromosomal localization of the neurological mouse mutations tottering (tg), Purkinje cell degeneration (pcd), and nervous (nr). Mol. Brain Res. 37 (1996), 79–84.
6. Canu, N., Tufi, R., Serafino, A.L., Amadoro, G., Ciotti, M.T., Calissano, P., Role of the autophagic-lysosomal system on low potassium-induced apoptosis in cultured cerebellar granule cells. J. Neurochem. 92 (2005), 1228–1242.
7. Castagna, C., Aimar, P., Alasia, S., Lossi, L., Post-natal development of the Reeler mouse cerebellum: an ultrastructural study. Ann. Anat. 196 (2014), 224–235.
8. Cendelin, J., From mice to men: lessons from mutant ataxic mice. Cerebellum Ataxias, 1, 2014, 4.
9. Chakrabarti, L., Eng, J., Ivanov, N., Garden, G.A., La Spada, A.R., Autophagy activation and enhanced mitophagy characterize the Purkinje cells of pcd mice prior to neuronal death. Mol. Brain, 2, 2009, 24.
10. Cheng, S.S., Heintz, N., Massive loss of mid- and hindbrain neurons during embryonic development of homozygous lurcher mice. J. Neurosci. 17 (1997), 2400–2407.
11. Christensen, H.M., Dikranian, K., Li, A., Baysac, K.C., Walls, K.C., Olney, J.W., Roth, K.A., Harris, D.A., A highly toxic cellular prion protein induces a novel nonapoptotic form of neuronal death. Am. J. Pathol. 176 (2010), 2695–2706.
12. Clarke, P.G.H., Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. 181 (1990), 195–213.
13. Cocito, C., Lossi, L., Merighi, A., A neurochemical study of the postnatal Reeler cerebellum. Front. Cell Neurosci., 2016 (submitted).
14. Colbourne, F., Sutherland, G.R., Auer, R.N., Electron microscopic evidence against apoptosis as the mechanism of neuronal death in global ischemia. J. Neurosci. 19 (1999), 4200–4210.
15. D'Arcangelo, G., Curran, T., Reeler: new tales on an old mutant mouse. Bioessays 20 (1998), 235–244.
16. D'Arcangelo, G., Miao, G.G., Chen, S.C., Soares, H.D., Morgan, J.I., Curran, T., A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374 (1995), 719–723.
17. D'Arcangelo, G., Miao, G.G., Curran, T., Detection of the reelin breakpoint in reeler mice. Brain Res. Mol Brain Res. 39 (1996), 234–236.
18. Dusart, I., Guenet, J., Sotelo, C., Purkinje cell death: dDifferences between developmental cell death and neurodegenerative death in mutant mice. Cerebellum 5 (2006), 163–173.
19. Falconer, D.S., Two new mutants ‘trembler’ and ‘reeler’, with neurological actions in the house mouse (Mus musculus L.). J. Genet. 50 (1951), 192–201.
20. Fernandez-Gonzalez, A., Spada, A.R.L., Treadaway, J., Higdon, J.C., Harris, B.S., Sidman, R.L., Morgan, J.I., Zuo, J., Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene, Nna1. Science 295 (2002), 1904–1906.
21. Goldowitz, D., Mullen, R.J., Granule cell as a site of gene action in the weaver mouse cerebellum: evidence from heterozygous mutant chimeras. J. Neurosci. 2 (1982), 1474–1485.
22. Hamilton, B.A., Frankel, W.N., Kerrebrock, A.W., Hawkins, T.L., FitzHugh, W., Kusumi, K., Russell, L.B., Mueller, K.L., van Berkel, V., Birren, B.W., Kruglyak, L., Lander, E.S., Disruption of the nuclear hormone receptor ROR[alpha] in staggerer mice. Nature 379 (1996), 736–739.
23. Heckroth, J.A., Goldowitz, D., Eisenman, L.M., Purkinje cell reduction in the reeler mutant mouse: a quantitative immunohistochemical study. J. Comp.Neurol. 279 (1989), 546–555.
24. Herrup, K., Busser, J.C., The induction of multiple cell cycle events precedes target-related neuronal death. Development 121 (1995), 2385–2395.
25. Herrup, K., Mullen, R.J., Role of the Staggerer gene in determining Purkinje cell number in the cerebellar cortex of mouse chimeras. Brain Res. 227 (1981), 475–485.
26. Herrup, K., Sunter, K., Numerical matching during cerebellar development: quantitative analysis of granule cell death in staggerer mouse chimeras. J. Neurosci. 7 (1987), 829–836.
27. Herrup, K., Trenkner, E., Regional differences in cytoarchitecture of the weaver cerebellum suggest a new model for weaver gene action. Neuroscience 23 (1987), 871–885.
28. Herrup, K., Mullen, R.J., Regional variation and absence of large neurons in the cerebellum of the staggerer mouse. Brain Res. 172 (1979), 1–12.
29. Herrup, K., Mullen, R.J., Staggerer chimeras: intrinsic nature of purkinje cell defects and implications for normal cerebellar development. Brain Res. 178 (1979), 443–457.
30. Katsuyama, Y., Terashima, T., Developmental anatomy of reeler mutant mouse. Dev., Growth Differ. 51 (2009), 271–286.
31. Klionsky, D.J., F.C. Abdalla, H. Abeliovich, R.T. Abraham, A. Acevedo-Arozena, K. Adeli, L. Agholme, M. Agnello, P. Agostinis, J.A. Aguirre-Ghiso, H.J. Ahn, O. Ait-Mohamed, S. Ait-Si-Ali, T. Akematsu, S. Akira, H.M. Al-Younes, M.A. Al-Zeer, M.L. Albert, R.L. Albin, J. Alegre-Abarrategui, M.F. Aleo, M. Alirezaei, A. Almasan, M. Almonte-Becerril, A. Amano, R.K. Amaravadi, S. Amarnath, A.O. Amer, N. Andrieu-Abadie, V. Anantharam, D.K. Ann, S. Anoopkumar-Dukie, H. Aoki, N. Apostolova, G. Arancia, J.P. Aris, K. Asanuma, N.Y. Asare, H. Ashida, V. Askanas, D.S. Askew, P. Auberger, M. Baba, S.K. Backues, E.H. Baehrecke, B.A. Bahr, X.Y. Bai, Y. Bailly, R. Baiocchi, G. Baldini, W. Balduini, A. Ballabio, B.A. Bamber, E.T. Bampton, G.+ Juh+ísz, C. R. Bartholomew, D.C. Bassham, R.C. Bast, H. Batoko, B.H. Bay, I. Beau, D.M. B+®chet, T.J. Begley, C. Behl, C. Behrends, S. Bekri, B. Bellaire, L.J. Bendall, L. Benetti, L. Berliocchi, H. Bernardi, F. Bernassola, S.+ Besteiro, I. Bhatia-Kissova, X. Bi, M. Biard-Piechaczyk, J.S. Blum, L.H. Boise, P. Bonaldo, D.L. Boone, B.C. Bornhauser, K.R. Bortoluci, I. Bossis, F. d. r. Bost, J.P. Bourquin, P. Boya, M. l. Boyer-Guittaut, P.V. Bozhkov, N.R. Brady, C. Brancolini, A. Brech, J.E. Brenman, A. Brennand, E.H. Bresnick, P. Brest, D. Bridges, M.L. Bristol, P.S. Brookes, E.J. Brown, J.H. Brumell, N. Brunetti-Pierri, U.T. Brunk, D.E. Bulman, S.J. Bultman, G. Bultynck, L.F. Burbulla, W. Bursch, J.P. Butchar, W. Buzgariu, S.P. Bydlowski, K. Cadwell, M. Cahov+í, D. Cai, J. Cai, Q. Cai, B. Calabretta, J. Calvo-Garrido, N. Camougrand, M. Campanella, J. Campos-Salinas, E. Candi, L. Cao, A.B. Caplan, S.R. Carding, S.M. Cardoso, J.S. Carew, C.R. Carlin, V. Carmignac, L.A. Carneiro, S. Carra, R.A. Caruso, G. Casari, C. Casas, R. Castino, E. Cebollero, F. Cecconi, J. Celli, H. Chaachouay, H.J. Chae, C.Y. Chai, D.C. Chan, E.Y. Chan, R.C.-C. Chang, C.M. Che, C.C. Chen, G.C. Chen, G.Q. Chen, M. Chen, Q. Chen, S.S. L. Chen, W. Chen, X. Chen, X. Chen, X. Chen, Y.G. Chen, Y. Chen, Y. Chen, Y.J. Chen, Z. Chen, A. Cheng, C.H. Cheng, Y. Cheng, H. Cheong, J.H. Cheong, S. Cherry, R. Chess-Williams, Z.H. Cheung, E. Chevet, H.L. Chiang, R. Chiarelli, T. Chiba, L.S. Chin, S.H. Chiou, F.V. Chisari, C.H. Cho, D.H. Cho, A.M. Choi, D. Choi, K.S. Choi, M.E. Choi, S. Chouaib, D. Choubey, V. Choubey, C.T. Chu, T.H. Chuang, S.H. Chueh, T. Chun, Y.J. Chwae, M.L. Chye, R. Ciarcia, M.R. Ciriolo, M.J. Clague, R.S. Clark, P.G. Clarke, R. Clarke, P. Codogno, H.A. Coller, M. a. I. Colombo, S. Comincini, M. Condello, F. Condorelli, M.R. Cookson, G.H. Coombs, I. Coppens, R. Corbalan, P. Cossart, P. Costelli, S. Costes, A. Coto-Montes, E. Couve, F.P. Coxon, J.M. Cregg, J.L. Crespo, M.J. Cronj+®, A.M. Cuervo, J.J. Cullen, M.J. Czaja, M. D'Amelio, A. Darfeuille-Michaud, L.M. Davids, F.E. Davies, M. De Felici, J.F. de Groot, C.A. de Haan, L. De Martino, A. De Milito, V. De Tata, J. Debnath, A. Degterev, B. Dehay, L.M. Delbridge, F. Demarchi, Y.Z. Deng, J.+ Dengjel, P. Dent, D. Denton, V. Deretic, S.D. Desai, R.J. Devenish, M. Di Gioacchino, G. Di Paolo, C. Di Pietro, G. D+¡az-Araya, I. s. D+¡az-Laviada, M.T. Diaz-Meco, J. Diaz-Nido, I. Dikic, S.P. Dinesh-Kumar, W.X. Ding, C.W. Distelhorst, A. Diwan, M. Djavaheri-Mergny, S. Dokudovskaya, Z. Dong, F.C. Dorsey. 2012. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8, 445–544.
32. Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J.i., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E., Tanaka, K., Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441 (2006), 880–884.
33. Komatsu, M., Waguri, S., Koike, M., Sou, Y.s., Ueno, T., Hara, T., Mizushima, N., Iwata, J.i., Ezaki, J., Murata, S., Hamazaki, J., Nishito, Y., Iemura, S.i., Natsume, T., Yanagawa, T., Uwayama, J., Warabi, E., Yoshida, H., Ishii, T., Kobayashi, A., Yamamoto, M., Yue, Z., Uchiyama, Y., Kominami, E., Tanaka, K., Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131 (2007), 1149–1163.
34. Komatsu, M., Wang, Q.J., Holstein, G.R., Friedrich, V.L., Iwata, J.i., Kominami, E., Chait, B.T., Tanaka, K., Yue, Z., Essential role for autophagy protein Atg7 in the maintenance of axonal homeostasis and the prevention of axonal degeneration. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 14489–14494.
35. Lambert de Rouvroit, C., Goffinet, A.M., The reeler mouse as a model of brain development. Adv. Anat. Embryol. Cell Biol. 150 (1998), 1–106.
36. Landis, D.M.D., Sidman, R.L., Electron microscopic analysis of postnatal histogenesis in the cerebellar cortex of staggerer mutant mice. J. Comp. Neurol. 179 (1978), 831–864.
37. Landis, S.C., Ultrastructural changes in the mitochondria of the cerebellar Purkinje cells of nervous mutant mice. J. Cell Biol. 57 (1973), 782–797.
38. Lee, J.A., Beigneux, A., Ahmad, S.T., Young, S.G., Gao, F.B., ESCRT-III dysfunction causes autophagosome accumulation and neurodegeneration. Curr. Biol. 17 (2007), 1561–1567.
39. Lewis, P.D., Cell death in the germinal layers of the postnatal rat brain. Neuropathol. Appl. Neurobiol. 1 (1975), 21–29.
40. Li, J., Yu, L., Gu, X., Ma, Y., Pasqualini, R., Arap, W., Snyder, E.Y., Sidman, R.L., Tissue plasminogen activator regulates Purkinje neuron development and survival. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 2410–2419.
41. Liberski, P.P., Brown, D.R., Sikorska, B., Caughey, B., Brown, P., Cell death and autophagy in prion diseases (transmissible spongiform encephalopathies). Folia Neuropathol. 46 (2008), 1–25.
42. Lossi, L., Castagna, C., Merighi, A., Neuronal cell death: an overview of its different forms in central and peripheral neurons. Lossi, L., Merighi, A., (eds.) Neuronal Cell Death, 2015, Springer, New York, 1–18.
43. Lossi, L., Gambino, G., Apoptosis of the cerebellar neurons. Histol. Histopathol. 23 (2008), 367–380.
44. Lossi, L., Gambino, G., Salio, C., Merighi, A., Autophagy regulates the post-translational cleavage of BCL-2 and promotes neuronal survival. Sci. World J. 10 (2010), 924–929.
45. Lossi, L., Merighi, A., In vivo cellular and molecular mechanisms of neuronal apoptosis in the mammalian CNS. Progr. Neurobiol. 69 (2003), 287–312.
46. Lossi, L., Mioletti, S., Merighi, A., Synapse-independent and synapse-dependent apoptosis of cerebellar granule cells in postnatal rabbits occur at two subsequent but partly overlapping developmental stages. Neurosci. 112 (2002), 509–523.
47. Lossi, L., Tamagno, I., Merighi, A., Molecular morphology of neuronal apoptosis: activation of caspase 3 during postnatal development of mouse cerebellar cortex. J. Mol. Histol. 35 (2004), 621–629.
48. Maiuri, M.C., Zalckvar, E., Kimchi, A., Kroemer, G., Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 8 (2007), 741–752.
49. Mariani, J., Crepel, F., Mikoshiba, K., Changeux, J.P., Sotelo, C., Anatomical, physiological and biochemical studies of the cerebellum from reeler mutant mouse. Philos. Trans. R. Soc. Lon. B. 281 (1977), 1–28.
50. Martin, L.J., Sieber, F.E., Traystman, R.J., Apoptosis and necrosis occur in separate neuronal populations in hippocampus and cerebellum after ischemia and are associated with differential alterations in metabotropic glutamate receptor signaling pathways. J. Cereb. Blood Flow Metab. 20 (2000), 153–167.
51. Marzban, H., Del Bigio, M.R., Alizadeh, J., Ghavami, S., Zachariah, R.M., Rastegar, M., Cellular commitment in the developing cerebellum. Front.Cell. Neurosci., 8, 2015, 450.
52. Migheli, A., Attanasio, A., Lee, W.H., Bayer, S.A., Ghetti, B., Detection of apoptosis in weaver cerebellum by electron microscopic in situ end-labeling of fragmented DNA. Neurosci. Lett. 199 (1995), 53–56.
53. Migheli, A., Piva, R., Wei, J., Attanasio, A., Casolino, S., Hodes, M.E., Dlouhy, S.R., Bayer, S.A., Ghetti, B., Diverse cell death pathways result from a single missense mutation in weaver mouse. Am. J. Pathol. 151 (1997), 1629–1638.
54. Mikoshiba, K., Nagaike, K., Kohsaka, S., Takamatsu, K., Aoki, E., Tsukada, Y., Developmental studies on the cerebellum from reeler mutant mouse in vivo and in vitro. Dev. Biol. 79 (1980), 64–80.
55. Moreno, S., Imbroglini, V., Ferraro, E., Bernardi, C., Romagnoli, A., Berrebi, A., Cecconi, F., Apoptosome impairment during development results in activation of an autophagy program in cerebral cortex. Apoptosis 11 (2006), 1595–1602.
56. Nishiyama, J., Yuzaki, M., Excitotoxicity and autophagy: Lurcher may not be a model of “autophagic cell death”. Autophagy 6 (2010), 568–570.
57. Nixon, R.A., The role of autophagy in neurodegenerative disease. Nat. Med. 19 (2013), 983–997.
58. Norman, D.J., Feng, L., Cheng, S.S., Gubbay, J., Chan, E., Heintz, N., The lurcher gene induces apoptotic death in cerebellar Purkinje cells. Development 121 (1995), 1183–1193.
59. Pamenter, M.E., Perkins, G.A., McGinness, A.K., Gu, X.Q., Ellisman, M.H., Haddad, G.G., Autophagy and apoptosis are differentially induced in neurons and astrocytes treated with an in vitro mimic of the ischemic penumbra. PLoS One, 7, 2012, 51469.
60. Patil, N., Cox, D.R., Bhat, D., Faham, M., Myers, R.M., Peterson, A.S., A potassium channel mutation in weaver mice implicates membrane excitability in granule cell differentiation. Nat. Genet. 11 (1995), 126–129.
61. Phillips, R.J.S., Lurcher”, a new gene in linkage group XI of the house mouse. J. Genet. 57 (1960), 35–42.
62. Rakic, P., Sidman, R.L., Weaver mutant mouse cerebellum: defective neuronal migration secondary to abnormality of Bergmann glia. Proc. Natl. Acad. Sci. U S A 70 (1973), 240–244.
63. Rami, A., Review: autophagy in neurodegeneration: firefighter and/or incendiarist?. Neuropathol. Appl. Neurobiol. 35 (2009), 449–461.
64. Schweichel, J.U., Merker, H.J., The morphology of various types of cell death in prenatal tissues. Teratology 7 (1973), 253–266.
65. Sidman, R.L., Lake, P.W., Dickie, M.M., Staggerer, a new mutation in the mouse affecting the cerebellum. Science 137 (1962), 610–612.
66. Smeyne, R.J., Goldowitz, D., Development and death of external granular layer cells in the weaver mouse cerebellum: a quantitative study. J. Neurosci. 9 (1989), 1608–1620.
67. Smeyne, R.J., Goldowitz, D., Purkinje cell loss is due to a direct action of the weaver gene in Purkinje cells: evidence from chimeric mice. Brain Res. Dev. Brain Res. 52 (1990), 211–218.
68. Tomoda, T., Bhatt, R.S., Kuroyanagi, H., Shirasawa, T., Hatten, M.E., A mouse serine/threonine kinase homologous to C. elegans UNC51 functions in parallel fiber formation of cerebellar granule neurons. Neuron 24 (1999), 833–846.
69. Triarhou, L.C., Biological clues on neuronal degeneration based on theoretical fits of decay patterns: towards a mathematical neuropathology. Folia Neuropathol. 48 (2010), 3–10.
70. Wei, L., Han, B.H., Li, Y., Keogh, C.L., Holtzman, D.M., Yu, S.P., Cell death mechanism and protective effect of erythropoietin after focal ischemia in the whisker-barrel cortex of neonatal rats. J. Pharmacol. Exp. Ther. 317 (2006), 109–116.
71. Won, S.J., Kim, S.H., Xie, L., Wang, Y., Mao, X.O., Jin, K., Greenberg, D.A., Reelin-deficient mice show impaired neurogenesis and increased stroke size. Exp. Neurol. 198 (2006), 250–259.
72. Wood, K.A., Dipasquale, B., Youle, R.J., In situ labeling of granule cells for apoptosis-associated DNA fragmentation reveals different mechanisms of cell loss in developing cerebellum. Neuron 11 (1993), 621–632.
73. Yamaguchi, Y., Miura, M., Programmed cell death in neurodevelopment. Dev. Cell 32 (2015), 478–490.
74. Yang, D.S., Kumar, A., Stavrides, P., Peterson, J., Peterhoff, C.M., Pawlik, M., Levy, E., Cataldo, A.M., Nixon, R.A., Neuronal apoptosis and autophagy cross talk in aging PS/APP Mice, a model of Alzheimer's disease. Am. J. Pathol. 173 (2008), 665–681.
75. Yuasa, S., Kitoh, J., Oda, S., Kawamura, K., Obstructed migration of Purkinje cells in the developing cerebellum of the reeler mutant mouse. Anat. Embryol. (Berl) 188 (1993), 317–329.
76. Yue, Z., Autophagy in lurcher mice: indicted but yet to be acquitted for the death of Purkinje cells. Autophagy 6 (2010), 571–572.
77. Yue, Z., Horton, A., Bravin, M., DeJager, P.L., Selimi, F., Heintz, N., A novel protein complex linking the +¦2 glutamate receptor and autophagy: implications for neurodegeneration in Lurcher mice. Neuron 35 (2002), 921–933.
78. Zuo, J., De Jager, P.L., Takahashi, K.A., Jiang, W., Linden, D.J., Heintz, N., Neurodegeneration in Lurcher mice caused by mutation in [delta]2 glutamate receptor gene. Nature 388 (1997), 769–773.