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Brushtail Possum) Two Stages of Increased IgA Transfer During Lactation in the Marsupial, Trichosurus vulpecula (Brushtail Possum) This information is current as Frances M. Adamski and Jerome Demmer of September 25, 2021. J Immunol 1999; 162:6009-6015; ; http://www.jimmunol.org/content/162/10/6009 Downloaded from References This article cites 35 articles, 11 of which you can access for free at: http://www.jimmunol.org/content/162/10/6009.full#ref-list-1 Why The JI? Submit online. http://www.jimmunol.org/ • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average by guest on September 25, 2021 Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 1999 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Two Stages of Increased IgA Transfer During Lactation in the Marsupial, Trichosurus vulpecula (Brushtail Possum)1,2 Frances M. Adamski3 and Jerome Demmer The polymeric Ig receptor (pIgR) and J chain molecules are involved in the transfer of IgA across the mammary gland epithelia into milk. The J chain binds two IgA molecules to form dimeric IgA, and the pIgR transports this complex through epithelial cells. We report here the cloning of the first marsupial homologues for the pIgR and J chain from the brushtail possum. Marsupial young are born after a short gestation and are less developed than eutherian newborn. The pouch young is completely dependent on milk as its sole source of nutrition during early lactation and this phase can be considered to be equivalent to an external gestation. Two periods of increased expression of pIgR, J chain, and IgA heavy chain mRNAs were observed in the mammary gland during lactation. The first occurs for a brief period after birth of the pouch young and is likely to reflect IgA transfer via the colostrum. The second period of increased expression, which is unique to marsupials, occurs after the early lactation period Downloaded from and just before young exit the pouch. We propose that this represents a second colostral-like phase at the end of the external gestation. The Journal of Immunology, 1999, 162: 6009–6015. arsupial young are born after a short gestation, which in the colostrum (7). For marsupials, little is known about Ig trans- in the possum is only 17 days (1). Their early pouch- fer via the placenta or mammary gland. In the newborn of several life is considered to be an external gestation as many marsupials, no Igs were detected in their serum until they had M http://www.jimmunol.org/ of the developmental changes that occur in utero for eutherian suckled for the first time, suggesting that in these species there is mammals take place during this time. In particular, lymphoid or- only postnatal transfer of Igs (8–10). In contrast, Igs have been gans of the marsupial neonate are immature and pouch young are detected in the serum of newborn of the tammar wallaby (Macro- unable to elicit an immune response for some time after birth (2, pus eugenii) before suckling (11). The transfer of Igs in utero has 3). Lactation in the brushtail possum extends for ;200 days, dur- not been investigated for the possum. It has been shown that new- ing which milk composition and the pouch young’s behavior born possums are unable to mount a humoral response for at least changes. In early lactation (first 80 days), the marsupial young is 14 days after birth (12). Thus postpartum transfer of both IgG and confined to the pouch where it remains attached to the nipple, IgA is likely to be important for immune protection of the possum receiving milk of unique protein, carbohydrate, mineral, and fat young. A study of three brushtail possums demonstrated that Igs by guest on September 25, 2021 composition (4–6). During the switch phase (days 80–120 of lac- ingested by 50- and 98- but not 145-day-old pouch young were tation), the milk composition changes to become similar in com- subsequently detected in their serum (13). This suggests that, al- position to that of eutherian mammals. With the change in milk though older pouch young can mount their own immune response, composition, growth of the pouch young increases, and they un- they remain receptive to the passive immunity offered by their dergo changes such as fur growth, their activity increases, suckling mothers milk, at least into the switch phase of lactation. is more intermittent (after day 80), and they begin to leave the Passively transferred IgA functions to protect mucus mem- pouch (after day 115). branes (respiratory and gastrointestinal) of the newborn. In euth- At birth, eutherian young are immunologically naive and they erian mammals, lymphocytes associated with mammary gland ep- receive immune protection by ingestion of Igs secreted into the ithelium secrete IgA as a dimer joined by the J chain (14). Dimeric colostrum until they are capable of mounting their own immune IgA is transported across the epithelial cells into the milk by the response. In mammals such as humans, where IgG is transferred polymeric Ig receptor (pIgR)4 and is released at the apical mem- predominately via the placenta, IgA is the major Ig transferred via brane by proteolytic cleavage of the extracellular domain (secre- the colostrum. In contrast, when little or no IgG is transferred tory component (SC)) (15). It has been suggested that the SC pro- before birth, as seen in the cow, more IgG than IgA is transferred tects dimeric IgA from proteolytic cleavage in mucosal environments (16). The possum IgA heavy chain (Ca) DNA se- Dairy Science Group, AgResearch, Ruakura Research Centre, Hamilton, New Zea- quence was published recently by Bevlov et al. (17). land Immune transfer to the possum neonate via the milk has not Received for publication October 7, 1998. Accepted for publication February been studied in great detail. In this work, we have cloned and 26, 1999. characterized the first marsupial homologues of the pIgR and J The costs of publication of this article were defrayed in part by the payment of page chain genes. Analysis of the expression pattern of the pIgR, J charges. This article must therefore be hereby marked advertisement in accordance chain, and Ca mRNA suggests that there are two stages of in- with 18 U.S.C. Section 1734 solely to indicate this fact. creased IgA transfer during lactation in the possum, after birth and 1 This work was supported by Ministry of Agriculture, and Forestry Policy, New Zealand, under contract PBC/09. during the switch phase. 2 All sequences reported have been deposited into the GenBank database, accession nos. AF091138 (polymeric Ig receptor), AF091138 (J chain), and AF091139– AF091141 (IgA heavy chain). 3 Address correspondence and reprint requests to Dr. Frances M. Adamski, Dairy 4 Abbreviations used in this paper: pIgR, polymeric Ig receptor; IgA heavy chain, Ca; Science Group, AgResearch, Ruakura Research Centre, Private Bag 3123, Hamilton, SC, secretory component; RACE, rapid amplification of cDNA end; CDR, comple- New Zealand. mentarity-determining region. Copyright © 1999 by The American Association of Immunologists 0022-1767/99/$02.00 6010 IgA TRANSFER DURING POSSUM LACTATION Materials and Methods with 32P-radiolabeled cDNA probes in Church and Gilbert hybridization 3 RNA purification solution (22) following 30 min prehybridization. Blots were washed in 2 SSC/0.1% SDS at 55°C, then 13 SSC/0.1% SDS for 20 min each. Blots Mammary gland total RNA. Mammary glands were collected as described were exposed to Kodak XAR-5 film (Rochester, NY) at 280°C with two previously (6), and the date of lactation was based on the size of the pouch intensifying screens. The possum 18S rRNA probe is an unpublished DNA young (18). The frozen mammary tissues were ground under liquid nitro- fragment (400 bp) amplified by RT-PCR (J. Demmer, GenBank gen by mortar and pestle, and RNA was extracted using the guanidinium AF089722). acid phenol chloroform method (19) with the modification of reducing the recommended amount of tissue per volume of reagent by one half. Results White blood cell total RNA. RBC were lysed by the addition of 12 ml of Isolation of possum pIgR gene lysis solution (150 mM NH4Cl, 10 mM KHCO3, and 0.1 mM EDTA) to 4.5 ml of heparin-treated possum blood, incubating on ice for 20 min. White A 156-bp DNA fragment corresponding to the possum pIgR was blood cells were harvested by centrifugation and washed with 13 PBS amplified by RT-PCR using mammary gland total RNA (28 days before RNA isolation as described above. lactation) and oligonucleotide primers designed to conserved re- RT-PCR and 59 rapid amplification of cDNA end (RACE) gions of the pIgR coding sequence. This fragment was used to screen an early lactation possum mammary gland cDNA library, Random or oligo-dT primed cDNA was generated using the Superscript and 12 positive cDNA clones were isolated. Of these, three re- preamplification system (Life Technologies, Gaithersburg, MD) as per the manufacturer’s instructions. PCR was performed using Platium Taq (Life combinants containing different-sized inserts were characterized Technologies) or Taq DNA polymerase (Boehringer Mannheim, Mann- by DNA sequencing.
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