Programmed cell death in the larval salivary glands of Apis mellifera (Hymenoptera, Apidae)

Journal of Biosciences

Volumn 32, Issue 2, 2007, Pages 309-328

  Silva Zacarin, E C M ^a   Tomaino, G A ^b   Brocheto Braga, M R ^b   Taboga, S R ^b   Silva De Moraes, R L M ^b  

^a FEDERAL UNIVERSITY OF SÃO CARLOS   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Degeneration; Honeybee; Larva; Prepupa; Silk gland

Indexed keywords

ACID PHOSPHATASE; BROMOPHENOL BLUE; DYE; EOSIN; HEMATOXYLIN; SILVER; URANYL ACETATE;

APOPTOSIS; BIOASSAY; CELL ORGANELLE; ENZYME ACTIVITY; HONEYBEE; LARVA; METAMORPHOSIS; PHOSPHATASE; RNA; SECRETION; TRANSMISSION ELECTRON MICROSCOPY;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL VACUOLE; CHEMICAL ANALYSIS; CONTROLLED STUDY; CYTOCHEMISTRY; CYTOPLASM; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME LOCALIZATION; EPITHELIUM CELL; GOLGI COMPLEX; HEMOLYMPH; HISTOCHEMISTRY; HONEYBEE; HYMENOPTERA; LARVAL DEVELOPMENT; LYSOSOME; METAMORPHOSIS; MICROSCOPY; MORPHOLOGICAL TRAIT; NONHUMAN; SALIVARY GLAND; TISSUE SECTION; TRANSMISSION ELECTRON MICROSCOPY;

ACID PHOSPHATASE; ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; BEES; HISTOCYTOCHEMISTRY; LARVA; METAMORPHOSIS, BIOLOGICAL; MICROSCOPY, ELECTRON, TRANSMISSION; SALIVARY GLANDS;

APIDAE; APIS MELLIFERA; HYMENOPTERA;

EID: 34248178220     PISSN: 02505991     EISSN: 02505991     Source Type: Journal    
DOI: 10.1007/s12038-007-0031-2     Document Type: Article

References (70)

1. Aidells B, Lockshin R A and Cullin A M 1971 Breakdown of the silk glands of Galleria mellonella - acid phosphatase in involuting glands; J. Insect Physiol. 17 857-869
2. Akai H 1984 The ultrastructure and functions of the silk gland cells of Bombyx mori; in Insect ultrastructure (eds) R C King, H Akai (New York: Plenum) vol. 2, pp 323-364
3. Armbruster L, Levy M, Mathieu M N and Bautz A M 1986 Acid phosphatase activity in the hemolymph, hemocytes, fat body and salivary glands during larval and prepupal development in Calliphora erythrocephala (Diptera: Calliphoridae); J. Biochem. Physiol. B84 349-354
4. Beaulaton J and Lockshin R A 1982 The relation of programmed cell death to development and reproduction. Comparative studies and an attempt at classification; Int. Rev. Cytol. 79 215-235
5. Biggiogera M, Bottone M G, Martin T E, Uchiumi T and Pellicciari C 1997 Still immunodetectable nuclear RNPs are extruded from the cytoplasm of spontaneously apoptotic thymocytes; Exp. Cell Res. 234 512-520
6. Biggiogera M, Bottone M G and Pellicciari C 1998 Nuclear RNA is extruded from apoptotic cells; J. Histochem. Cytochem. 46 999-1005
7. Bowen I D 1984 Laboratory technique for demonstrating cell death; in Cell ageing and death (eds) I Davies and D C Sigee (Cambridge: Cambridge University Press) pp 1-38
8. Bowen I D, Hollander J E and Lewis G H J 1982 Cell death and acid phosphatase activity in the regenerating planarian Polycelis tenuis; Differentiation 21 160-170
9. Bowen I D, Morgan S M and Mullarkey K 1993 Cell death in the salivary glands of metamorphosing Calliphora vomitoria; Cell Biol. Int. 17 13-33
10. Bowen I D, Mullarkey K and Morgan S M 1996 Programmed cell death in the salivary gland of the blow fly Calliphora vomitoria; Microsc. Res. Tech. 34 202-217
11. Bowen I D and Ryder T A 1976 Use of the p-nitrophenyl phosphate method for the demonstration of acid phosphatase during starvation and cell autolysis in the planarian Polycelis tenuis Iijima; Histochem. J. 8 319-329
12. Bursch W, Kleine L and Tenniswood M 1990 Biochemistry of cell death by apoptosis; Biochem. Cell. Biol. 68 1071-1074
13. Clavaguera A, Querol E and Coll D 1983 Cytochemical studies on the nature of NOR (nucleolus organizer region) silver stainability; Cell. Mol. Biol. 29 255-259
14. Costa R A C and Cruz-Landim C 2001 Distribution of acid phosphatases in the hypopharyngeal glands from workers, queens and males of a Brazilian stingless bee Scaptotrigona postica Latreille: an ultrastructural cytochemical study; Histochem. J. 33 653-662
15. Cruz-Landim C and Mello M L S 1967 The post-embryonic changes in Melipona quadrifasciata anthidioides Lep (Hymenoptera, Apoidea); J. Morphol. 123 481-502
16. Cruz-Landim C and Melo R A 1981 Desenvolvimento e Envelhecimento de larvas e adultos de Scaptotrigona postica latreille (Hymenoptera, Apidae): aspectos histológicos e histoquímicos (São Paulo, Brazil: ACIESP)
17. Cruz-Landim C and Silva de Moraes R L M 1977 Estruturas degenerativas nas glândulas hipofaríngeas de operárias de Apis mellifera (Apidae); Rev. Brasil. Biol. 37 681-692
18. Cruz-Landim C and Silva de Moraes R L M 2000 Morte Celular Programada em abelhas como uma forma de redirecionar a morfologia e a fisiologia adaptativa (Rio Claro, SP: Editora e tipografia Costa)
19. Dai J D and Gilbert L I 1999 An in vitro analysis of ecdysteroidelicited cell death in the prothoracic gland of Manduca sexta; Cell Tissue Res. 297 319-327
20. Dorstyn L, Colussi P A and Quinn L M 1999 DRONC, an ecdysone-inducible Drosophila caspase; Proc. Natl. Acad. Sci. USA 96 4307-4312
21. Eeken J C J 1977 Ultrastructure of salivary glands of Drosophila lebanonensis during normal development and after in vivo ecdysterone administration; J. Insect Physiol. 23 1043-1055
22. Ferguson D J and Anderson T J 1981 Ultrastructural observation on cell death by apoptosis in the "resting" human breast; Virchows Arch. Pathol. Anat. Histopathol. 393 193-203
23. Flower N E and Kenchington W 1967 Studies on insect fibrous proteins: the larval silk of Apis, Bombus and Vespa; J. Roy. Micro. Soc. 86 297-310
24. Hacker G 2000 The morphology of apoptosis; Cell Tissue Res. 301 5-17
25. Howell W M and Black D A 1980 Controlled silver staining of nucleolus organizer regions with protective colloidal developer: I-step method; Experientia 36 104-105
26. Jochová J, Zakeri Z and Lockshin R A 1997a Rearrangement of the tubulin and actin cytoskeleton during programmed cell death in Drosophila salivary glands; Cell Death Differ. 4 140-149
27. Jochová J, Quaglino D, Zakeri Z, Woo K, Sikorska M, Weaver V and Lockshin R 1997b Protein synthesis, DNA degradation, and morphological changes during programmed cell death in labial glands of Manduca sexta; Dev. Genet. 21 249-257
28. Jones H 1990 Programmed cell death in the larval salivary glands of Drosophila melanogaster, PhD thesis, University of Wales College of Cardiff, Cardiff, Wales, UK
29. Jones G W and Bowen I D 1980 The fine structural localization of acid phosphatase in pore cells of embryonic and newly hatched Deroceras reticulatum (Pulmonata: Stylonimatophora); Cell Tissue Res. 204 253-265
30. Jones H E and Bowen I D 1993 Acid phosphatase activity in the larval salivary glands of developing Drosophila melanogaster; Cell Biol. Int. 17 305-315
31. Jurand A and Pavan C 1975 Ultrastructural aspects of histolytic processes in the salivary gland cells during metamorphic stages in Rhynchosciara hollaenderi (Diptera, Sciaridae); Cell Differ. 4 219-236
32. Kerr J F R, Willie A H and Currie A R 1972 Apoptosis, a basic biological phenomenon with wider ranging implications in tissue kinetics; Br. J. Cancer 24 239-257
33. Kloetzel J A and Laufer H 1969 A fine-structure analysis of larval salivary gland function in Chironomus thummi (Diptera); J. Ultrastruct. Res. 29 15-36
34. Kondo T, Takeuchi K and Doi Y 1997 ERM (ezrin/radixin/moesin)-based molecular mechanism of microvillar breakdown at an early stage of apoptosis; J. Cell Biol. 139 749-758
35. Laicine E M, Fernandez M A and Sawaia H 1991 Acid phosphatase activity in mature secretory granules of the salivary gland of Bradysia hygida; J. Morphol. 208 247-255
36. Lee C Y and Baehrecke E H 2001 Steroid regulation of autophagic programmed cell death during development; Development 128 1443-1455
37. Levy M and Bautz A M 1985 Degeneration of larval salivary glands during metamorphosis of the blow-fly Calliphora erythrocephala Meigen (Diptera: Calliphoridae); Int. J. Insect Morphol. Embryol. 14 281-290
38. Lewis G H J and Bowen I D 1985 A methacrylate embedding technique for combined autoradiography and acid phosphatase histochemistry; Histochem. J. 17 467-475
39. Lockshin R A 1981 Cell death in metamorphosis; in Cell death in biology and pathology (eds) I D Bowen and R A Lockshin (London: Chapmam and Hall) pp 79-121
40. Lockshin R A and Zakeri Z F 1994 Programmed cell death: early changes in metamorphosing cells; Biochem. Cell Biol. 72 589-596
41. Lockshin R A and Zakeri Z 2004 Caspase-independent cell death?; Oncogene 23 2766-2773
42. Lockshin R A, Zakeri Z and Tilly J L 1998 When cells die (Canada: Wiley-Liss)
43. Matsuura S, Morimoto T and Nagata S 1968 Studies on the posterior silk gland of the silkworm, Bombyx mori. II - Cytolytic processes in posterior silk gland cells during metamorphosis from larva to pupa; J. Cell Biol. 38 589-603
44. Mello M L S, Vidal B C, Dantas M M and Monteiro A L P 1993 Discrimination of the nucleolus by a critical electrolyte concentration method; Acta Histochem. Cytochem. 26 1-3
45. Mills J C, Stone N L and Erhardt J 1998 Apoptotic membrane blebbing is regulated by myosin light chain phosphorylation; J. Cell Biol. 140 627-636
46. Morimoto T, Matsuura S and Nagata S 1968 Studies on the posterior silk gland of the silkworm, Bombyx mori. III. Ultrastructural changes of the posterior silk gland cells in the fourth larval instar; J. Cell Biol. 38 604-614
47. Myohara M 2004. Real-time observation of autophagic programmed cell death of Drosophila salivary glands in vitro; Dev. Genes Evol. 214 99-104
48. Pearse A G E 1960 Histochemistry, theoretical and applied (London: Jet Churchill)
49. Pollard J W, Pacey J and Cheng S V Y 1987 Estrogens and cell death in murine uterine luminal epithelium; Cell Tissue Res. 249 533-540
50. Pratt R M and Greene R M 1976 Inhibition of palatal epithelial cell death by altered protein synthesis; Dev. Biol. 54 135-145
51. Ryder T A and Bowen I D 1975 A method for the fine structural localization of acid phosphatase activity using p-nitrophenyl phosphate as substrate; J. Histochem. Cytochem. 23 235-237
52. Schin K S and Laufer H 1973 Studies of programmed salivary gland regression during larval-pupal transformation in Chironomus thummi; Exp. Cell Res. 82 335-340
53. Sedmak J J and Grossberg S E 1977 A rapid, sensitive and versatile assay for protein using Coomassie Brilliant Blue G-250; Anal. Biochem. 79 544-552
54. Sehnal F and Akai H 1990 Insect silk glands: their types, development and function, and effects of environmental factors and morphogenetic hormones on them; Int. J. Insect Morphol. Embryol. 19 79-132
55. Sehnal F and Akai H 1982 Ultrastructure and function of silk glands in Galleria mellonella; in The ultrastructure and functioning of cells (eds) H Akai, R C King and S Morohoshi (Tokyo: Soc. for Insect Cells Japan) pp 135-138
56. Sehnal F, Janda V Jr and Nemec V 1983 Composition, synthetic and cytolytic activities of Galleria mellonella silk glands during the last-larval instar under the action of juvenile hormone; J. Insect Physiol. 29 237-248
57. Shiba H, Uchida D, Kobayashi H and Natori M 2001 Involvement of cathepsin B- and L-like proteinases in silk gland histolysis during metamorphosis of Bombyx mori; Arch. Biochem. Biophys. 390 28-34.
58. Silva de Moraes R L M 1977 Comportamento nuclear em glândulas salivares de Melipona quadrifasciata anthidioides Lep. durante o desenvolvimento larval; Papéis Avul. Zool. 31 49-77
59. Silva de Moraes R L M and Bowen I D 2000 Modes of cell death in the hypopharyngeal gland of the honey bee (Apis mellifera L.); Cell Biol. Int. 24 737-743
60. Silva de Moraes R L M and Cruz-Landim C 1979 Estudos ultraestruturais da glândula salivar larval de Melipona quadrifasciata anthidioides Lep. durante o desenvolvimento larval; Rev. Brasil. Biol. 39 103-116
61. Silva de Moraes R L M and Cruz-Landim C 1980 Ultraestrutura das glândulas salivares larvais de Pseudohypocera kertezi (Enderlein, 1912) (Diptera, Phoridae); Dusenia 12 95-104
62. Silva E C M and Silva de Moraes R L M 2002 Cell and secretion functional differentiation of Apis mellifera silk glands; Naturalia 27 29-45
63. Silva-Zacarin E C M, Silva de Moraes R L M and Taboga S R 2003 Silk formation mechanisms in the larval salivary glands of Apis mellifera (Hymenoptera: Apidae); J. Biosci. 28 753-764
64. Tashiro Y, Morimoto T and Matsuura S 1968 Studies on the posterior gland of the silkworm, Bombyx mori. I. Growth of posterior silk gland cells and biosynthesis of fibroin during the fifth larval instar; J. Cell Biol. 38 574-588
65. Trump B F and Mergner W J 1974 Cell injury; in The inflammatory process (eds) B W Zurrisfach, L Grant and R T McCusky (New York: Academic Press) pp 209-242
66. Vidal B C, Barbisan L F, Maria S S, Russo J and Mello M L S 1996 Apoptosis: identification by a critical eletrolyte concentration method; Apoptosis 1 218-221
67. Wyllie A H 1981 Cell death: a new classification separating apoptosis from necrosis; in Cell death in biology and pathology (eds) I D Bowen and R A Lockshin (New York: Chapman and Hall) pp 9-34
68. Zakeri Z, Quaglino D, Latham T and Lockshin R A 1993 Delayed internucleosomal DNA fragmentation in programmed cell death; FASEB J. 7 470-478
69. Zar J H 1999. Biostatistical analysis (New Jersey: Prentice Hall, Englewood Cliffs)
70. Zara F J and Caetano F H 2002 Ultrastructure of salivary glands of Pachycondyla (=Neoponera) villosa (Fabricius) (Formicidae: Ponerinae): functional changes during the last larval instar; Cytologia 67 267-280