A megalin-like receptor is involved in protein endocytosis in the midgut of an insect (Bombyx mori, Lepidoptera)

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 295, Issue 4, 2008, Pages

  Casartelli, M ^a   Cermenati, G ^a   Rodighiero, S ^b   Pennacchio, F ^c   Giordana, B ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b Centro Interdisciplinare di Materiali e Interfacce Nanostrutturati (CIMaINa)   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Albumin endocytosis; Clathrin mediated endocytosis; Columnar cells in culture; Lepidopteran larval midgut; Megalin

Indexed keywords

ALBUMIN; FLUORESCEIN ISOTHIOCYANATE; GENTAMICIN; MEGALIN;

ARTICLE; CELL CULTURE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DRUG INHIBITION; ENDOCYTOSIS; EPITHELIUM CELL; LEPIDOPTERA; MIDGUT; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TEMPERATURE SENSITIVITY;

2,4-DINITROPHENOL; ANIMALS; ARSENICALS; BOMBYX; CELLS, CULTURED; CHLORPROMAZINE; CLATHRIN; COLD TEMPERATURE; CYTOCHALASIN B; DIETARY PROTEINS; EDETIC ACID; ENDOCYTOSIS; FLUORESCEIN-5-ISOTHIOCYANATE; GASTROINTESTINAL TRACT; GENE EXPRESSION; GENTAMICINS; INSECT PROTEINS; LDL-RECEPTOR RELATED PROTEIN 2; MICROFILAMENTS; MICROTUBULES; NOCODAZOLE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, NUCLEIC ACID; SERUM ALBUMIN; SODIUM AZIDE; TEMPERATURE;

EID: 57349193454     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00036.2008     Document Type: Article

References (59)

1. Allingham PG, Kerlin RL, Tellam RL, Briscoe SJ, Standfast HA. Passage of host immunoglobulin across the mid-gut epithelium into the haemolymph of blood-fed buffalo flies Haematobia irritans exigua. J Insect Physiol 38: 9-17, 1992.
2. Apodaca G. Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic 2: 149-159, 2001.
3. Ben-Yakir D, Shochat C. The fate of immunoglobulin G fed to larvae of Ostrinia nubilalis. Entomol Exp Appl 81: 1-5, 1996.
4. 12 and binds receptor-associated protein. J Biol Chem 272: 26497-26504, 1997.
5. Birn H, Zhai XY, Holm J, Hansen SI, Jacobsen C, Christensen EI, Moestrup SK. Megalin binds and mediates cellular internalization of folate binding protein. FEBS J 272: 4423-4430, 2005.
6. Blackburn MB, Loeb MJ, Clark E, Jaffe H. Stimulation of midgut stem cell proliferation by Manduca sexta α--Arylphorin. Arch Insect Biochem Physiol 55: 26-32, 2004.
7. Bradford MM. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
8. Caccia S, Casartelli M, Grimaldi A, Losa E, Pennacchio F, de Eguileor M, Giordana B. The unexpected similarity of intestinal sugar absorption by SGLT1 and apical GLUT2 in an insect and in mammals. Am J Physiol Regul Integr Comp Physiol 292: R2284-R2291, 2007.
9. Casartelli M, Corti P, Leonardi MG, Fiandra L, Burlini N, Pennacchio F, Giordana B. Absorption of albumin by the midgut of a lepidopteran larva. J Insect Physiol 51: 933-940, 2005.
10. Casartelli M, Corti P, Cermenati G, Grimaldi A, Fiandra L, Santo N, Pennacchio F, Giordana B. Absorption of horseradish peroxidase in Bombyx mori larval midgut. J Insect Physiol 53: 517-525, 2007.
11. Casida JE, Quistad GB. Golden age of insecticide research: past, present, or future? Annu Rev Entomol 43: 1-16, 1998.
12. Cermenati G, Corti P, Caccia S, Giordana B, Casartelli M. A morphological and functional characterization of Bombyx mori larval midgut cells in culture. Invert Survival J 4: 119-126, 2007.
13. Choi JS, Kim KR, Ahn DW, Park YS. Cadmium inhibits albumin endocytosis in opossum kidney epithelial cells. Toxicol Appl Pharmacol 161: 146-152, 1999.
14. Christensen EI, Gliemann J, Moestrup SK. Renal tubule gp330 is a calcium binding receptor for endocytic uptake of protein. J Histochem Cytochem 40: 1481-1490, 1992.
15. Christensen EI, Birn H. Megalin and cubilin: multifunctional endocytic receptors. Nat Rev Mol Cell Biol 3: 258-268, 2002.
16. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature 422: 37-44, 2003.
17. Dallai R, Lupetti P, Lane NJ. The organization of actin in the apical region of insect midgut cells after deep etching. J Struct Biol 122: 283-292, 1998.
18. Down RE, Fitches EC, Wiles DP, Corti P, Bell HA, Gatehouse JA, Edwards JP. Insecticidal spider venom toxin fused to snowdrop lectin is toxic to the peach-potato aphid, Myzus persicae (Hemiptera: Aphididae) and the rice brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Pest Manag Sci 62: 77-85, 2006.
19. Elkjaer ML, Birn H, Agre P, Christensen EI, Nielsen S. Effects of microtubule disruption on endocytosis, membrane recycling and polarized distribution of aquaporin-1 and gp330 in proximal tubule cells. Eur J Cell Biol 67: 57-72, 1995.
20. Ellinger I, Rothe A, Grill M, Fuchs R. Apical to basolateral transcytosis and apical recycling of immunoglobulin G in trophoblast-derived BeWo cells: effects of low temperature, nocodazole and cytochalasine D. Exp Cell Res 269: 322-331, 2001.
21. Fishman L, Zlotkin E. A diffusional route of transport of horseradish peroxidase through the midgut of a fleshfly. J Exp Zool 229: 189-195, 1984.
22. Fitches E, Woodhouse SD, Edwards JP, Gatehouse JA. In vitro and in vivo binding of snowdrop (Glantus nivalis agglutinin; GNA) and jackbean (Canavalia ensiformis; Con A) lectins within tomato moth (Lacanobia oleracea) larvae; mechanism of insecticidal action. J Insect Physiol 47: 777-787, 2001.
23. Fitches E, Edwards MG, Mee C, Grishin E, Gatehouse Angharad MR, Edwards JP, Gatehouse JA. Fusion proteins containing insect-specific toxins as pest control agents: snowdrop lectin delivers fused insecticidal spider venom toxin to insect haemolymph following oral ingestion. J Insect Physiol 50: 61-71, 2004.
24. m of albumin receptor-mediated endocytosis in OK cells. Am J Physiol Renal Fluid Electrolyte Physiol 268: F899-F906, 1995.
25. Gekle M, Mildenberger S, Freudinger R, Silbernagl S. Functional characterization of albumin binding to the apical membrane of OK cells. Am J Physiol Renal Fluid Electrolyte Physiol 271: F286-F291, 1996.
26. Gekle M, Mildenberger S, Freudinger R, Schwerdt G, Silbernagl S. Albumin endocytosis in OK cells: dependence on actin and microtubules and regulation by protein kinase. Am J Physiol Renal Physiol 272: F668-F677, 1997.
27. Gekle M, Mildenberger S, Freudinger R, Silbernagl S. Long-term protein exposure reduces albumin binding and uptake in proximal tubule-derived opossum kidney cells. J Am Soc Nephrol 9: 960-968, 1998.
28. Gekle M. Renal tubule albumin transport. Annu Rev Physiol 67: 573-594, 2005.
29. Habibi J, Brandt SL, Coudron TA, Wagner RM, Wright MK, Backus EA, Huesing JE. Uptake, flow and digestion of casein and green fluorescent protein in the digestive system of Lygus hesperus Knight. Arch Insect Biochem Physiol 50: 62-74, 2002.
30. Hakim RS, Blackburn MB, Corti P, Gelman DB, Goodman C, Elsen K, Loeb MJ, Lynn D, Soin T, Smagghe G. Growth and mitogenic effects of arylphorin in vivo and in vitro. Arch Insect Biochem Physiol 64: 63-73, 2007.
31. Hamm-Alvarez SF, Sonee M, Loran-Goss K, Shen WC. Paclitaxel and nocodazole differentially alter endocytosis in cultured cells. Pharm Res 13: 1647-1656, 1996.
32. Herz J, Bock HH. Lipoprotein receptors in the nervous system. Annu Rev Biochem 71: 405-434, 2002.
33. Hunyady L, Merelli F, Baukal AJ, Balla T, Catt KJ. Agonist-induced endocytosis and signal generation in adrenal glomerulosa cells. J Biol Chem 266: 2783-2788, 1991.
34. Jeffers LA, Thompson DM, Ben-Yakir D, Roe RM. Movement of proteins across the digestive system of the tobacco budworm, Heliothis virescens. Entomol Exp Appl 117: 135-146, 2005.
35. Kaksonen M, Sun Y, Drubin DG. A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115: 475-487, 2003.
36. Kaksonen M, Toret CP, Drubin DG. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 7: 404-414, 2006.
37. Kurahashi H, Atiwetin P, Nagaoka S, Miyata S, Kitajiama S, Sugimura Y. Absorption of mulberry root urease to the hemolymph of the silkworm, Bombyx mori. J Insect Physiol 51: 1055-1061, 2005.
38. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685, 1970.
39. Lehane MJ. Digestion and fate of the vertebrate bloodmeal in insects. In: The Immunology of Host-Ectoparasitic Arthropod Relationships, edited by Wikel SK. Wallingford, UK: CABI, 1996.
40. Loeb MJ, Hakim RS. Insect midgut epithelium in vitro: an insect stem cell system. J Insect Physiol 42: 1103-1111, 1996.
41. McCarthy RA, Barth JL, Chintalapudi MR, Knaak C, Argraves WS. Megalin functions as an endocytotic sonic hedgehog receptor. J Biol Chem 277: 25660-25667, 2002.
42. Moestrup SK, Cui S, Vorum H, Bregengard C, Bjorn SE, Norris K, Gliemann J, Christensen EI. Evidence that epithelial glycoprotein 330/megalin mediates uptake of polybasic drugs. J Clin Invest 96: 1404-1413, 1995.
43. Moestrup SK, Verroust PJ. Megalin- and cubilin-mediated endocytosis of protein-bound vitamins, lipids and hormones in polarized epithelia. Annu Rev Nutr 21: 407-428, 2001.
44. Murray JW, Wolkoff AW. Roles of the cytoskeleton and motor proteins in endocytic sorting. Adv Drug Deliv Rev 55: 1385-1403, 2003.
45. Pitterle DM, Sperling RT, Myers MG, White MF, Blackshear PJ. Early biochemical events in insulin-stimulated fluid phase endocytosis. Am J Physiol Endocrinol Metab 276: E94-E105, 1999.
46. Powell KS, Spence J, Bharathi M, Gatehouse JH, Gatehouse Angharad MR. Immunohistochemical and developmental studies to elucidate the mechanism of action of the snowdrop lectin on the rice brown planthopper, Nilaparvata lugens (Stal). J Insect Physiol 44: 529-539, 1998.
47. Sadrud-Din SY, Hakim RS, Loeb MJ. Proliferation and differentiation of midgut cells from Manduca sexta, in vitro. Invert Reprod Dev 26: 197-204, 1994.
48. Sadrud-Din SY, Loeb MJ, Hakim RS. In vitro differentiation of isolated stem cells from the midgut of Manduca sexta larvae. J Exp Biol 199: 319-325, 1996.
49. Saito A, Pietromonaco S, Loo AK, Farquhar MG. Complete cloning and sequencing of rat gp330/megalin, a distinctive member of the low density lipoprotein receptor gene famaly. Proc Natl Acad Sci USA 91: 9725-9729, 1994.
50. Smith MG, Swamy SR, Pon LA. The life cycle of actin patches in mating yeast. J Cell Sci 114: 1505-1513, 2001.
51. Smythe E, Ayscough KR. Actin regulation in endocytosis. J Cell Sci 119: 4589-4598, 2006.
52. Takano M, Nakanishi N, Kitahara Y, Sasaki Y, Murakami T, Nagai J. Cisplatin-induced ihibition of receptor-mediated endocytosis of protein in the kidney. Kidney Int 62: 1707-1717, 2002.
53. Tuma PL, Hubbard AL. Transcytosis: crossing cellular barriers. Physiol Rev 83: 871-932, 2003.
54. Wang LH, Rothberg KG, Anderson RGW. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol 123: 1107-1117, 1993.
55. Waschke J, Drenckhahn D. Uniform apicobasal polarity of microtubules and apical location of -tubulin in polarized intestinal epithelium in situ. Eur J Cell Biol 79: 317-326, 2000.
56. Whetstone PA, Hammock BD. Delivery methods for peptide and protein toxins in insect control. Toxicon 49: 576-596, 2007.
57. Yammani RR, Seetharam S, Seetharam B. Cubilin and megalin expression and their interaction in the rat intestine: effect of thyroidectomy. Am J Physiol Endocrinol Metab 281: E900-E907, 2001.
58. Yarar D, Waterman-Storer CM, Schmid SL. A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell 16: 964-975, 2005.
59. Yochem J, Tuck S, Greenwald I, Han M. A gp330/megalin-related protein is required in the major epidermis of Caenorhabditis elegans for completion of molting. Development 126: 597-606, 1999.