Veterinarski arhiv 69 2

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VETERINARSKI ARHIV = 69 (2),=20 97-103, 1999

ISSN 1331-8055 Published = in=20 Croatia

Isolation of carp = (Cyprinus=20 carpio L.) intestinal intraepithelial lymphocytes

Frane Bozic* =

Department of = Pharmacology and=20 Toxicology, Faculty of Veterinary Medicine,
University of Zagreb, = Zagreb,=20 Croatia

* Contact = address:
Frane Bozic, DVM,=20
Department of Pharmacology and Toxicology, Veterinary Faculty, = University of=20 Zagreb, Heinzelova 55, 10000 Zagreb, Croatia,
Phone: 385 1 23 90 = 163; Fax:=20 385-1-214-697; E-mail: bozic@mavef.vef.hr

BOZIC, F.: Isolation = of carp=20 (Cyprinus carpio L.) intestinal intraepithelial lymphocytes. Vet. = arhiv=20 69, 97-103, 1999.

ABSTRACT =

The described procedure = is a simple and=20 rapid method for isolating pure lymphocytes from carp gut epithelium. = The=20 advantage of the described technique of i-IELs extraction is that it = allows for=20 the extraction of the cells from each carp, making it possible to study = their=20 characteristics on an individual basis in fish. In this procedure, gut=20 intraepithelial lymphocytes are separated from the epithelium layer and = other=20 lymphoid cells by Percoll gradient centrifugation. Since this procedure = results=20 in high recovery and purity in a preparation of i-IELs , there is no = need for=20 multiple nylon wool filtrations. The obtained i-IELs population could be = utilised for molecular, biochemical or phenotypic characterisation, as = well as=20 for functional evaluation, such as proliferative and cytotoxic = activities.=20

Key words: carp, = intraepithelial=20 lymphocytes, gut, fish

Introduction =

Mammal gut-associated = lymphoid tissue=20 (GALT) comprises three major lymphoid areas: Peyer's patches (PP), = lamina=20 propria (LP) and an intraepithelial compartment, which contains the=20 intraepithelial lymphocytes (IEL). It is well known that PP and LP cells = contain=20 more than 40% of B cells and a large percentage of CD4⁺ T = cells.=20 Additionally, lymphocyte populations of the PP and LP continuously = re-circulate=20 in the blood and lymphatic systems.

On the other hand, = intestinal=20 intraepithelial lymphocytes (i-IELs) undergo minimal re-circulation and = do not=20 require the thymus for their maturation (POUSSIER and JULIUS, 1994), = which=20 suggests that their role is specific for their tissue site. The majority = of=20 i-IELs in all vertebrates (in rodents, through chickens to humans) = express=20 CD8⁺ (suppressor/cytotoxic) phenotype (ERNST et al., 1986). = Also,=20 i-IELs contain high percentages (approximately 30-50%) of T cells = expressing=20 gdTCR (LEFRANCOIS, 1991), whereas gdTCR is present on approximately 5% of thymocytes = and=20 circulating T cells, except in calves, where peripheral blood = lymphocytes=20 express more than 20% gdTCR (WATERS et al., = 1995).=20

While the i-IELs precise = biologic=20 functions remain enigmatic, numerous findings made during the past few = years=20 demonstrate that mammal i-IELs may participate in immunity (FINDLY et = al., 1993;=20 MOMBAERTS et al., 1993; BOZIC et al., 1998) as well as in non-immune = functions=20 (BOISMENU and HAVRAN, 1994; 1997; BOISMENU et al., 1996).

Apart from numerous = differences in the=20 immune system between mammals and lower vertebrates, notably fish = (MANNING,=20 1994; RAST et al., 1997; MAGOR and VASTA, 1998), i-IELs obviously exist = in the=20 gut of teleosts (HART et al., 1986, 1988; ROMBOUT et al., 1993). Indeed, = i-IELs=20 have recently been isolated from carp gut (ROMBOUT et al., 1998) and it = seems=20 likely that this gut lymphocytes population represent a very large = number of=20 putative T cell types. However, the procedure of isolation has not been=20 described comprehensively. Therefore, we describe a simple and rapid = technique=20 for isolation of carp i-IELs in detail here.

Materials and = methods=20

Fish

Twelve-month-old carp, = Cyprinus=20 carpio L., with initial masses of approximately 200 g, were kept in = an=20 aquarium (100 l) under laboratory conditions in running, filtered tap = water with=20 constant flow rate and temperature (19=B11 =B0C). The fish were fed = daily with=20 commercially prepared pellet food (Ribnjak "Berlek", Ptuj, Slovenia), = amounting=20 to 2% of their body mass. Ten fish were used in the experiment. =

Necropsy = procedures

After euthanasia by = spinal rupture, the=20 gut was excised for isolation of intestinal intraepithelial lymphocytes. = In=20 order to isolate i-IELs, immediately after excision, collected = intestines were=20 placed in a tissue culture medium (TCM), consisting of RPMI 1640 without = Ca²⁺/Mg²⁺, plus 10% foetal calf serum (FCS). =

Percoll solutions =

For separation of i-IELs = from=20 enterocytes and other cell types, the material was centrifugated in = Percoll=20 gradients. Before the preparation of Percoll gradients, it must be = prepared in a=20 stock solution. A 1=D7 stock solution was used by mixing 90 ml Percoll = (Sigma)=20 with 10 ml of 10 =D7 phosphate-buffered saline (PBS). These solutions = must be=20 freshly prepared.

For 40% Percoll a = solution was mixed=20 consisting of 40 ml of 1=D7 stock solution and 60 ml RPMI 1640 without=20 Ca²⁺/Mg²⁺. Also, for a 70% Percoll solution, 70 ml = of 1=D7=20 stock solution and 30 ml RPMI 1640 was mixed without=20 Ca²⁺/Mg²⁺.

Harvesting of carp = i-IELs=20

Intestinal = intraepithelial lymphocytes=20 were isolated from carp gut by a modified procedure previously described = for=20 rodents i-IEL isolation (LEVENTON et al., 1983; MOSLEY and KLEIN, 1992;=20 LEFRANCOIS, 1993). This procedure was adapted to the fish system. After = fish=20 euthanasia, proximal and distal segments of gut were removed from one = individual=20 carp and were placed in a Petri dish containing RPMI 1640 plus 10% FCS.=20 Intestines were held in forceps and the tip of a 20-G-needle with = syringe filled=20 with cold TCM, was forced into the lumen between forceps, flushing the = entire=20 gut thoroughly in TCM to remove faecal material, with 30 ml (total) cold = TCM.=20 Intestines were replaced in a Petri dish containing fresh TCM and = connective=20 tissue was removed from intestinal samples. Gut samples were cut = longitudinally,=20 and then into small segments, 1-1.5 cm in length. These segments were = then=20 transferred to 50-ml conical tubes with 40 ml cold PBS without=20 Ca²⁺/Mg²⁺ and were washed by inverting the tubes = several=20 times. This step was repeated three times. The intestinal pieces were = then=20 transferred into a 100-ml Erlenmeyer flask containing 80 ml PBS without=20 Ca²⁺/Mg²⁺, plus 1 mM ethylenediamine tetraacetic = acid=20 disodium salt (EDTA) (Sigma). The samples were stirred in this solution = for 30=20 min at 37 ⁰C. The solution, together with gut pieces, was = then=20 transferred to a 50-ml conical centrifuge tube and vortexed for 10 sec = at=20 maximum setting. When the pieces had settled, the supernatant was = transferred to=20 another 50-ml conical tube and pelleted by centrifugation (400 =D7 = g for 8=20 min). Remaining intestinal tissues were then removed. The collected = pellet was=20 re-suspended in 40% Percoll (Sigma). The cells in the 40% Percoll (10 = ml) were=20 overlaid onto 2 ml of 70% Percoll solution, placed in a 15-ml conical = tube and=20 i-IELs were separated from enterocytes by centrifugation (600 =D7 = g for 20=20 min) at room temperature. The top half of the gradient was aspirated to = within=20 approximately 2 cm of the interface and i-IELs were then harvested from = 40:70=20 interface with a Pasteur pipette. Cells were diluted 1:3 with cold RPMI = 1640=20 without Ca²⁺/Mg²⁺, and centrifugated for 8 min at = 800 =D7=20 g to pellet. The purified i-IELs (> 96% pure) were more than = 98%=20 viable as determined by 0.2% trypan blue exclusion staining. Freshly = isolated=20 i-IELs were enumerated under a light microscope.

Results =

It is evident that there = was an=20 abundant number of i-IELs in the gut of carp. The quantity mean (=B1 SD) = of i-IEL=20 collected from one individual carp used in the basic protocol was 5.0 = =B1 0.4 =D7=20 10⁷ for proximal and second gut segment. The mean (=B1 SD) = number of=20 viable cells was 4.9 =B1 0.5 =D7 10⁷. Although the count was = variable=20 depending on the initial amount of intestinal mucous, probably due to = individual=20 differences, the yield of i-IEL was generally consistent between = different=20 extractions (Fig. 1). Purity exceeded 96% (contamination due to = epithelial and=20 other cells was negligible) and viability was over 98%, as determined = with=20 trypan blue exclusion staining.
<= BR=20 clear=3Dall>
Fig. 1. Recovery of = intraepithelial=20 lymphocytes from the proximal and distal gut of carp. Absolute number = obtained=20 from individual fish (N=3D10) revealed consistency between different = i-IEL=20 extractions.

Discussion =

The described procedure = is a simple and=20 rapid method for isolating extremely pure lymphocytes from carp gut = epithelium.=20 The advantage of the described technique of i-IELs extraction is that it = allows=20 for extraction of cells from carp on a per fish basis. Thus, a large = amount of=20 i-IELs can be obtained from individual fish, making it possible to study = their=20 characteristics on an individual basis. It is important to note that the = high=20 reproducibility was observed after centrifugation of cells in Percoll = gradients=20 at 600 =D7 g for 20 min or at 1500 =D7 g for 30 min, as = has been=20 previously proposed (ROMBOUT et al., 1998). The obtained absolute number = of=20 i-IELs in this current study was, however, significantly smaller than = i-IEL=20 numbers recently isolated from carp gut epithelium by others (ROMBOUT et = al.,=20 1998). These differences in the numbers of lymphocytes are probably due = to=20 techniques of i-IELs isolation. Namely, the present i-IELs extraction = procedure=20 differs from the i-IEL isolation method performed by ROMBOUT et al. = (1998), in=20 that the lamina propria remained intact after digestion of the = epithelium=20 (MOSLEY and KLEIN, 1992), but scraping off gut mucosa from the = underlying tissue=20 could cause damage to the lamina propria and subsequently result in=20 contamination from lymphocytes in that compartment and resulting in a = greater=20 number of cells in i-IEL preparation (our unpublished results). = Additionally, it=20 is important that procedures of i-IEL isolation do not penetrate into = the lamina=20 propria also, due to changes in the phenotype of i-IELs (ERNST et al., = 1986).=20

This study provides = evidence that, in=20 contrast to higher vertebrates, the gut of carp contains more intestinal = intraepithelial lymphocytes, although the higher vertebrates, such as = calves,=20 possess a larger population of lymphocytes within their intestinal = epithelium=20 (WATERS et al., 1995) than do carp. However, this is not the case in = rodents,=20 such as mice and rats. The i-IEL yield was found to be variable for = these rodent=20 species, not exceeding 15 x 10⁶ in rats (TEITELBAUM et al., = 1995) and=20 10 x 10⁶ in mice (LEVENTON et al., 1983; MOSLEY and KLEIN, = 1992;=20 LEFRANCOIS, 1993). We consider the abundant i-IEL numbers recovered by = the=20 procedure described here and elsewhere (ROMBOUT et al., 1998) to be an = important=20 immunological hallmark in teleost fish. Together with excessive mucous=20 production, compared to higher vertebrates, a very large population of = i-IEL=20 could benefit fish survival in a non-hostile aquatic environment. = Interestingly,=20 preliminary observations in this laboratory indicated that a certain = drop in=20 i-IEL numbers could be accompanied by enteropathy found in stressed = carp.=20

Despite the numerical = importance of=20 carp i-IELs, and the fact that they arise in the immediate vicinity of = the=20 largest permanent antigenic stimulus in the whole organism, data on = their=20 origin, site of development and phenotypic characteristics, are = generally=20 lacking. Indeed, the gdTCR⁺ = CD8⁺=20 T cells in i-IEL of carp (ROMBOUT et al., 1998) have recently been = suggested.=20

In conclusion, the = abundant number of=20 carp i-IELs, as a possible front line of defence at epithelial barriers, = could=20 constitute an excellent model system for novel, functional studies of = fish=20 immunity, with the aim of benefitting aquaculture. Also, fish i-IELs = represent a=20 potential model system for comparative studies of immunology, which = could assist=20 in unravelling the complexities of the mammalian immune system. =

References =

BOISMENU, R., W. L. = HAVRAN (1994):=20 Modulation of epithelial cell growth by intraepithelial gd T cells. Science. 266, 1253-1255.

BOISMENU, R., L. FENG, Y. = Y. XIA, J. C.=20 C. CHANG, W. L. HAVRAN (1996): Chemokine expression by intraepithelial = gd T cells. J. Immunol. 157, 985-992.

BOISMENU, R., W. L. = HAVRAN (1997): An=20 innate view of gd T cells. Curr. Opin. = Immunol. 9,=20 57-63.

BOZIC, F., D. FORCIC, R. = MAZURAN, A.=20 MARINCULIC, Z. KOZARIC, D. STOJCEVIC (1998): gdTCR⁺ intestinal intraepithelial = lymphocytes=20 (i-IEL) in reaction against intestinal nematode Trichinella = spiralis.=20 Comp. Immun. Microbiol. Infect. Dis. 21, 201-214.

ERNST, P. B., D. A. = CLARK, K. L.=20 ROSENTHAL, D. A. BEFUS, J. BIENENSTOCK (1986): Detection and = characterization of=20 cytotoxic T lymphocyte precursors in the murine intestinal = intraepithelial=20 leukocyte population. J. Immunol. 136, 2121-2126.

FINDLY, R. C., S. J. = ROBERTS, A. C.=20 HAYDAY (1993): Dynamic response of murine gut intraepithelial T-cells = after=20 infection by the coccidian parasite Eimeria. Eur. J. Immunol. 23, = 2557-2564.

HART, S., A. B. = WRATHMELL, J. E. HARRIS=20 (1986): Ontogeny of gut-associated lymphoid tissue (GALT) in the dogfish = Scyliorhinus canicula L. Vet. Immunol. Immunopathol.12, 107-116.=20

HART, S., A. B. = WRATHMELL, J. E.=20 HARRIS, T. H. GRAYSON (1988): Gut immunology in fish: a rewiev. Dev. = Comp.=20 Immunol. 12, 453-480.

LEFRANCOIS, L. (1991): = Phenotypic=20 complexity of intraepithelial lymphocytes of the small intestine. J. = Immunol.=20 147, 1746-1751.

LEFRANCOIS, L. (1993): = Isolation of=20 mouse small intestinal intraepithelial lymphocytes. Curr. Protoc. = Immunol.=20 (suppl. 6), 3.19.1. - 3.19.7.

LEVENTON, G. S., S. S. = KULKARNI, M. L.=20 MEISTRICH, J. R. NEWLAND, A. R. ZANDER (1983): Isolation of small bowel=20 intraepithelial lymphocytes. J. Immunol. Meth. 63, 35-44.

MAGOR, K. E., G. R. VASTA = (1998):=20 Ancestral immunity comes of age. Immunol. Today. 19, 54-56.

MANNING, M. J. (1994): = Fishes. In:=20 Immunology (Turner, R. J., Ed.). A Comparative Approach. John Wiley = & Sons=20 Ltd. pp. 69-100.

MOMBAERTS, P., J. = ARNOLDI, F. RUSS=20 (1993): Different roles of ab and gd T-cells in immunity against an intracellular = bacterial=20 pathogen. Nature 365, 53-56.

MOSLEY, R. L., J. R. = KLEIN (1992): A=20 rapid method for isolating murine intestine intraepithelial lymphocytes = with=20 high yield and purity. J. Immunol. Meth. 156, 19-26.

POUSSIER, P., M. JULIUS = (1994): Thymus=20 indenpendent T cell development and selection in the intestinal = epithelium. Ann.=20 Rev. Immunol. 12, 521-553.

RAST, J. P., M. K. = ANDERSON, S. J.=20 STRONG, C. LEUR, R. T. LITMAN, G. W. LITMAN (1997): a,=20 b, g and d T cell antigen receptor genes arose early in = vertebrate=20 phylogeny. Immunity 6, 1-11.

ROMBOUT, J. H. W. M., A. = J.=20 TAVERNE-THIELE, M. I. VILLENA (1993): The gut-associated lymphoid tissue = (GALT)=20 of carp (Cyprinus carpio L.): an immunocytochemical analysis. = Dev. Comp.=20 Immunol. 17, 55-66.

ROMBOUT, J. H. W. M., P. = H. M. JOOSTEN,=20 A. P. ENGLESMA, N. VOSTAVERNE-THIELE, J. J. TAVERNE-THIELE (1998): = Indications=20 for a distinct putative T cell population in mucosal tissue of carp = (Cyprinus=20 carpio L.). Dev. Comp. Immunol. 22, 63-77.

TEITELBAUM, D. H., B. = NEIDECK, J. LEE,=20 R. MERION (1995): Inhibitory activity of intestinal intraepithelial = lymphocytes.=20 Surgery 118, 378-384.

WATERS, W. R., J. A. = HARP, B. J.=20 NONNECKE (1995): Phenotypic analysis of peripheral blood lymphocytes and = intestinal intra-epithelial lymphocytes in calves. Vet. Immunol. = Immunopathol.=20 48, 249-259.

Received: 2 November = 1998
Accepted:=20 10 April 1999

BOZIC, F.: = Izdvajanje=20 intraepitelnih limfocita iz crijeva sarana (Cyprinus carpio = L.). Vet.=20 arhiv 69, 97-103, 1999.

SAZETAK =

Opisani postupak = jednostavna je i brza=20 metoda za izolaciju cistih limfocita iz crijevnoga epitela =9Aarana. = Prednost=20 opisane metode izdvajanja limfocita je u tome =9Ato se njome moze = izdvojiti=20 dostatan broj stanica iz samo jedne ribe. Crijevni intraepitelni = limfociti=20 razdvojeni su od epitelijalnih elemenata i ostalih limfnih stanica=20 centrifugiranjem u gradijentu gustoce Perkola. Radi velikoga broja i = iznimne=20 cistoce izoliranih stanica, nepotrebno je proci=9Acavanje filtracijom = kroz=20 vi=9Aeslojnu najlonsku vunu. Dobivena populacija crijevnih = intraepitelnih=20 limfocita moze se rabiti u svrhu molekulske, biokemijske ili fenotipske = analize,=20 jednako kao i za istrazivanje njihove funkcijske uloge, primjerice = proliferacije=20 i citotoksicnosti.

Kljucne rijeci: = =9Aaran,=20 intraepitelni limfociti, crijevo, ribe

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