Abstract
AbstractSecretory immunoglobulin (Ig) A is a decameric Ig composed of four α-heavy chains, four light chains, a joining (J) chain, and a secretory component (SC). The heavy and light chains form two tetrameric Ig molecules that are joined by the J chain and associate with the SC. Expression of a secretory monoclonal antibody in tobacco (Nicotiana tabacum) has been described: this molecule (secretory IgA/G [SIgA/G]) was modified by having a hybrid heavy chain sequence consisting of IgG γ-chain domains linked to constant region domains of an IgA α-chain. In tobacco, about 70% of the protein assembles to its final, decameric structure. We show here that SIgA/G assembly and secretion are slow, with only approximately 10% of the newly synthesized molecules being secreted after 24 h and the bulk probably remaining in the endoplasmic reticulum. In addition, a proportion of SIgA/G is delivered to the vacuole as at least partially assembled molecules by a process that is blocked by the membrane traffic inhibitor brefeldin A. Neither the SC nor the J chain are responsible for vacuolar delivery, because IgA/G tetramers have the same fate. The parent IgG tetrameric molecule, containing wild-type γ-heavy chains, is instead secreted rapidly and efficiently. This strongly suggests that intracellular retention and vacuolar delivery of IgA/G is due to the α-domains present in the hybrid α/γ-heavy chains and indicates that the plant secretory system may partially deliver to the vacuole recombinant proteins expected to be secreted.
References
44
Referenced
68
10.1104/pp.120.4.961
/ Plant Physiol / Delivery of a secreted soluble protein to the vacuole via a membrane anchor. by Barrieu (1999){'key': '2021062510461931700_R2', 'first-page': '1145', 'article-title': 'A carboxyl-terminal propeptide is necessary for proper sorting of barley lectin to vacuoles of tobacco.', 'volume': '2', 'author': 'Bednarek', 'year': '1990', 'journal-title': 'Plant Cell'}
/ Plant Cell / A carboxyl-terminal propeptide is necessary for proper sorting of barley lectin to vacuoles of tobacco. by Bednarek (1990)10.1046/j.1365-313X.1998.00208.x
/ Plant J / Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. by Boevink (1998){'key': '2021062510461931700_R4', 'first-page': '507', 'article-title': 'ER protein quality control and proteasome-mediated protein degradation.', 'volume': '10', 'author': 'Brodsky', 'year': '1999', 'journal-title': 'Cell Dev Biol'}
/ Cell Dev Biol / ER protein quality control and proteasome-mediated protein degradation. by Brodsky (1999)10.1091/mbc.11.1.217
/ Mol Biol Cell / Dissociation from BiP and retrotranslocation of unassembled immunoglobulin light chains are tightly coupled to proteasome activity. by Chillaron (2000){'key': '2021062510461931700_R6', 'first-page': '2335', 'article-title': 'The maize γ-zein sequesters α-zein and stabilizes its accumulation in protein bodies of transgenic tobacco endosperm.', 'volume': '8', 'author': 'Coleman', 'year': '1996', 'journal-title': 'Plant Cell'}
/ Plant Cell / The maize γ-zein sequesters α-zein and stabilizes its accumulation in protein bodies of transgenic tobacco endosperm. by Coleman (1996)10.1023/A:1006029617949
/ Plant Mol Biol / Compartment-specific accumulation of recombinant immunoglobulins in plant cells: an essential tool for antibody production and immunomodulation of physiological functions and pathogen activity. by Conrad (1998)10.1105/tpc.11.11.2233
/ Plant Cell / Saturation of the endoplasmic reticulum retention machinery reveals anterograde bulk flow. by Crofts (1999){'key': '2021062510461931700_R9', 'first-page': '51', 'article-title': 'Protein secretion in plant cells can occur via a default pathway.', 'volume': '2', 'author': 'Denecke', 'year': '1990', 'journal-title': 'Plant Cell'}
/ Plant Cell / Protein secretion in plant cells can occur via a default pathway. by Denecke (1990)10.1007/978-94-011-0511-8_34
/ Plant Molecular Biology Manual / Targeting of proteins to the vacuole. by Dombrowski (1994){'key': '2021062510461931700_R11', 'first-page': '587', 'article-title': 'Determination of the functional elements within the vacuolar targeting signal of barley lectin.', 'volume': '5', 'author': 'Dombrowski', 'year': '1993', 'journal-title': 'Plant Cell'}
/ Plant Cell / Determination of the functional elements within the vacuolar targeting signal of barley lectin. by Dombrowski (1993)10.1105/tpc.10.6.1031
/ Plant Cell / Sorting of phaseolin to the vacuole is saturable and requires a short C-terminal peptide. by Frigerio (1998)10.1083/jcb.93.1.97
/ J Cell Biol / Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. by Fujiki (1982)10.2307/3869631
/ Plant Cell / Tonoplast and soluble vacuolar proteins are targeted by different mechanisms. by Gomez (1993)10.1002/eji.1830241033
/ Eur J Immunol / The efficiency of cysteine-mediated intracellular retention determines the differential fate of secretory IgA and IgM in B and plasma cells. by Guenzi (1994)10.1038/342076a0
/ Nature / Production of antibodies in transgenic plants. by Hiatt (1989)10.1093/jxb/48.1.139
/ J Exp Bot / Isolation of prolegumin from developing pea seeds: its binding to endomembranes and assembly into prolegumin hexamers in the protein storage vacuole. by Hinz (1997)10.1083/jcb.135.3.623
/ J Cell Biol / A pathway for targeting soluble misfolded proteins to the yeast vacuole. by Hong (1996)10.1104/pp.96.1.18
/ Plant Physiol / The signal peptide of a vacuolar protein is necessary and sufficient for the efficient secretion of a cytosolic protein. by Hunt (1991)10.1016/S0167-7799(00)89016-2
/ Trends Biotechnol / Immunotherapeutic potential of antibodies produced in plants. by Ma (1995)10.1126/science.7732380
/ Science / Generation and assembly of secretory antibodies in plants. by Ma (1995)10.1038/nm0598-601
/ Nat Med / Characterization of a recombinant plant monoclonal secretory antibody and preventive immunotherapy in humans. by Ma (1998)10.1002/eji.1830240120
/ Eur J Immunol / Assembly of monoclonal antibodies with IgG1 and IgA heavy chain domains in transgenic tobacco plants. by Ma (1994)10.1096/fasebj.14.5.769
/ FASEB J / Degradation of unassembled soluble Ig subunits by cytosolic proteasomes: evidence that retrotranslocation and degradation are coupled events. by Mancini (2000)10.1105/tpc.11.4.587
/ Plant Cell / Plant vacuoles. by Marty (1999)10.1083/jcb.130.6.1307
/ J Cell Biol / Different sensitivity to wortmannin of two vacuolar sorting signals indicates the presence of distinct sorting machineries in tobacco cells. by Matsuoka (1995)10.1073/pnas.88.3.834
/ Proc Natl Acad Sci USA / Propeptide of a precursor to a plant vacuolar protein required for vacuolar targeting. by Matsuoka (1991)10.1016/S0065-2776(08)60240-0
/ Adv Immunol / Immunoglobulin A (IgA): molecular and cellular interactions involved in IgA biosynthesis and immune response. by Mestecky (1987)10.1023/A:1006032627036
/ Plant Mol Biol / Sorting of proteins to vacuoles in plant cells. by Neuhaus (1998){'key': '2021062510461931700_R30', 'first-page': '1869', 'article-title': 'Protein quality control along the route to the plant vacuole.', 'volume': '9', 'author': 'Pedrazzini', 'year': '1997', 'journal-title': 'Plant Cell'}
/ Plant Cell / Protein quality control along the route to the plant vacuole. by Pedrazzini (1997)10.1046/j.1365-313X.1994.5010103.x
/ Plant J / Binding of BiP to an assembly-defective protein in plant cells. by Pedrazzini (1994)10.1073/pnas.93.9.4207
/ Proc Natl Acad Sci USA / A mutant cytochrome b 5 with a lengthened membrane anchor escapes from the endoplasmic reticulum and reaches the plasma membrane. by Pedrazzini (1996)10.1007/BF00203660
/ Planta / Degradation of transport-competent destabilized phaseolin with a signal for retention in the endoplasmic reticulum occurs in the vacuole. by Pueyo (1995)10.1093/jxb/49.326.1463
/ J Exp Bot / The protein N-glycosylation in plants. by Rayon (1998)10.1007/BF01089036
/ Planta / Cellular localization of nodule-enhanced aspartate aminotransferase in Medicago sativa L. by Robinson (1994){'key': '2021062510461931700_R36', 'first-page': '695', 'article-title': 'Different legumin protein domains act as vacuolar targeting signals.', 'volume': '3', 'author': 'Saalbach', 'year': '1991', 'journal-title': 'Plant Cell'}
/ Plant Cell / Different legumin protein domains act as vacuolar targeting signals. by Saalbach (1991)10.1105/tpc.11.4.629
/ Plant Cell / The specificity of vesicle trafficking: coat proteins and SNAREs. by Sanderfoot (1999)10.1104/pp.101.2.451
/ Plant Physiol / Colocalization of barley lectin and sporamin in vacuoles of transgenic tobacco plants. by Schroeder (1993)10.1016/0092-8674(90)90092-S
/ Cell / Developmental regulation of IgM secretion: the role of the carboxy-terminal cysteine. by Sitia (1990)10.2527/1995.7392752x
/ J Anim Sci / A biotechnological approach to improving the nutritive value of alfalfa. by Tabe (1995)10.4049/jimmunol.112.3.949
/ J Immunol / Studies on the structural and conformational basis for the relative resistance of serum and secretory immunoglobulin A to proteolysis. by Underdown (1974){'key': '2021062510461931700_R42', 'first-page': '615', 'article-title': 'The endoplasmic reticulum: gateway of the secretory pathway.', 'volume': '11', 'author': 'Vitale', 'year': '1999', 'journal-title': 'Plant Cell'}
/ Plant Cell / The endoplasmic reticulum: gateway of the secretory pathway. by Vitale (1999)10.1016/S1360-1385(99)01389-8
/ Trends Plant Sci / What do proteins need to reach different vacuoles? by Vitale (1999)10.1046/j.1365-313X.1992.t01-41-00999.x
/ Plant J / Vicilin with carboxy-terminal KDEL is retained in the endoplasmic reticulum and accumulates to high levels in the leaves of transgenic plants. by Wandelt (1992)
Dates
Type | When |
---|---|
Created | 23 years, 1 month ago (July 27, 2002, 1:01 a.m.) |
Deposited | 1 year, 7 months ago (Jan. 5, 2024, 8:06 a.m.) |
Indexed | 4 weeks, 1 day ago (Aug. 5, 2025, 9:10 a.m.) |
Issued | 25 years, 1 month ago (Aug. 1, 2000) |
Published | 25 years, 1 month ago (Aug. 1, 2000) |
Published Online | 25 years, 1 month ago (Aug. 1, 2000) |
Published Print | 25 years, 1 month ago (Aug. 1, 2000) |
@article{Frigerio_2000, title={Assembly, Secretion, and Vacuolar Delivery of a Hybrid Immunoglobulin in Plants}, volume={123}, ISSN={0032-0889}, url={http://dx.doi.org/10.1104/pp.123.4.1483}, DOI={10.1104/pp.123.4.1483}, number={4}, journal={Plant Physiology}, publisher={Oxford University Press (OUP)}, author={Frigerio, Lorenzo and Vine, Nicholas D. and Pedrazzini, Emanuela and Hein, Mich B. and Wang, Fei and Ma, Julian K.-C. and Vitale, Alessandro}, year={2000}, month=aug, pages={1483–1494} }