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Phylogeny of Thymus and Bone Marrow - Bursa Cells, R.K. Wright and E.L. Cooper eds.
@ Elsevier/North-Holland Biomedical Press, Amsterdam, The Netherlands



                             THE IIEUATOGENIC TISSUES OF TIJNICATES



                                        Thomas H. Ernak
                                .   DepartmenL of Physlology
                           Unlver.sltY of Callfornia !tredical Center
                                San Fiancisco, Cal-lfornla 94143



INTRODUCTIOTiI

    Tunlcates are unique among lnvertebrates in that they share such chordaLe
characterl-stics as a notochord, dorsal tubul-ar nerve cord, and pharyngeal- gill
slits with the vertebrates.           The ascidlans, a group of sessile tmicates'        are

generally considered to have glven rLse Lo the vertebrates via a pelaglc tadpole
latval.                                                       feeding mrlne
            RecenLly, biol-ogists have turned toward these fllter
                                                                        3' 4'
animals 1n an attempt to understand the origin of the lunune t""pot"t2'
Speclal- attention has focused on the ascidian lynphocyte, a relatively               undiffer-

entiated cell that l-s comon to all ascldian species and generates all other
                   6'7.   circulatlng lF'phocytes are reported to participate ln
blood ce1l ayp."5,
 the rejectlon of allografts2,          fot rosettes wlth sheep red blood cells8,       and

 respond to phytohenagglutinlng.
    ByautoradiograPhywlthtrltiatedthyflidine,bloodcel].sengagedlnPremitotic
 DNA  synthesis have been localized Ln the tlssue s of Stgela "7"n"IO. Ascidian
 bl-ood cells, which constitute a renewing ceL1 populatlon' proliferate in clrcu-

 lating blood and in lyaph nodules throughout the body' The ultrastructure of
                                                                      12' 13 b.a toa
 several- types of bl-ood celLs has been described in blood "p".."ll'
 in a lynph nodule. For thLs study, a postlarval ascldian Juvenile and several
                                                          15' 16 for a short time
 adul-t ascldians were exposed to tritlated thyrnldinel4'
 l-nterval in order to localize sites of hematoge[ic activlty.                In StgeTa clava,

 the organlzation of a pharyngeal          Lymph nodul"e was exanined      by electron micros-

 copy"           the putative   DNA   synthesizing ce1ls described'
          "nd


 HEMATOGENESIS      IN A   POSTLARVAL JUVENILE

     The Ciona intestinalis         juvenile (Fig. 1) is considered to most closely


                                                   45
6

                                                                                    i'
                                        L9
resemble the ancestral ascidi-"rr18'          and is essentially a sirnpltf ied adult.
Af   ter metamorphosis, it has a beati-ng heart , a si-ngle incurrent siphon,                two

widely spaced excurrent siphons,      and    a pair of primitive gill       slits        (protostig-
mata) on each side of the ph"ryrr*2o.         The gut loop lies slightly       behind and to the
left of the pharynx.
     Numerous hemocytoblasts, undlfferentiated       ce1ls hrith a large, nucl"eolated
nucleus and little    basophil-lc cytoplasm, and a few presmbly             differentiated           ce11s

cluster in the pharyngeal wall around the protostigmata and near the endostyle.
Hemocytoblasts originate fron cel1s of the archent..or2l               and are especlalLy

numerous below germinal cells in the stignatlc          eplthellul[.      Clusters of these
prinitive    blood celLs do not occur around the postpharyngeal gut.                 In autoradio-
grams, hemocytoblasts are labeled with tritlated          thymidine (fig. 2).             With
continued dlvislon and by nlgratlon,         the pharyngeal hemocytoblasts w111 give rise
to henatogenLc tissue in the pharynx and around the gut of an adult Cjona.                          They

will probably also suppty gerninal cel-Is for the ovary and testis22.


DISTRIBUTION OI' I{EMATOGENIC SITES    IN   ADIJI,T ASCIDIANS

     In adult ascidians, the pharynx is a greatly enlarged organ perforated by                       a

multltude of ciliated    gill   s11ts (stigmata).     HemaLogenlc tissue occurs 1n the

pharyngeal wa1l, around the di-gestive tract,        and anong advanced solitary              species,
ln the body walI,     Each ascidian fanlly     exhiblts a characteristic            relationshlp
befween pharynx, postpharyogeal gut (esophagus, stomach, and intestlne),                      and

gonads, and the distrLbution of henatogenic tlssue foLlows accordingly.

     An adult Ciona intestinal.is   has several of the most prinltlve          ascidian body
features.    The postpharyngeal gut lies slightly       behind the pharlmx, and the
gonads f-ie withln the curvature of the dlgestive tract.               Hematogenic tissue ls

abundant in the pharyngeal wa1l and around the gut-l-oop. A few clueters also

occur in the body lralf at the posterlor end of the body6 and where the pharynx i.s
attached to the body wa11, either under the endostyle or by mesenteries. Except
in these reglons, blood formlng tissue is absent from the body              wa11.

     Henatogenic cel-le Ln the pharynx of Ciona are abundant ln transverse bars
47



(Flg. 3) and scattered in longitudinal bars and al-ong the endostyle. Blood cells
are arranged 1n smalJ-, diffuse clusters adjacent to the pharyngeal ePitheliun;
ce11s labeled vlth trirlated      thymidine are scattered throughout the tissue (Fig.
4).    Most non-dividing cel1s are presumed to be Partially       or fu1ly differentiated
blood cells.     Around the gut, hematogenic tj-ssue is aLso diffuse and associated

wlth connectlve tissue or the external gut linlng.         Clustered blood cells may be
so plentiful    as to 1ie cLose to the stomach ePltheliun.       In regions rthere the
gonads are present, hemaEogenic tissue is sparse.

      Ta cheTgosona productum and Ascidia ceratodes, other solltaly      ascidians    whose

gonads lie within the gut LooP' most hemtogenic tissue ls around the gut and

organized into sna1l nodules containing several cel-ls whlch incorPorate tritiated
thynidlne.     Lynph nodules are assoclated with connective tissue and blood chan-

nels but not the external or internal gut eplthelial         nodules also frequently occur

near the gonade.
      The gut-loop of most colonial ascldlans is U-shaped and lies behind the

pharyu, a delLcate structure contalning lLtt1e hernatogenlc tissue.           In

PoTgcTinum p-lanum and Euherd.nania cTavitotmis, clusters of labeled blood celLs

are most abundant in the region of the gut-loop where they occur Ln small Patches
ln the connective tlssue and adjacent to the eplcardium, a singl,e pouch alongsLde
the gut but not llning it.
      The gonads of advanced sPecles 1le withln the body wall'      and it Ls only ln

these specles that lynph nodules are abundant ln this regl-on. In StgeJ.a          c-Zava'

nost lynph nodules occur 1n the pharyngeal and body walls; few occur around the
                 .10
postpharyngeal gut--.        Although no nodules have bee4 observed below the stomach

eplthellurn, a ferr scattered ones are seen in the connectlve tissue around the
intestinal     epitheliun.    Lymph nodules 1n the body wall l"le next to the atrial

epithelLum and in the connectlve tissue linlng blood channels (Fig. 5)'            Some


nodules also occur in the endocarps, projections of the atrial         epltheliun filled

with connective tissue and blood cells.          In Stye-la, a nodule conslsts of one or

two groups of ce1ls Labeled wlth trltiated         thynidine surrounded by several un-

labeled ce11s. Many of the        DNA   syntheslzing ceLl-s are hemocytoblasts with   a
4


dj-sLinct nucleolus.      In lftolgufa verrucifera and Pguza haustot, where both the gut
and gonads lie withl-n the body wa1l, distlnct        l,ynph nodules occur both in the

connectlve tlssue and adjacent to the atrlal         epitheLLun. In the connective
tissue, nodules frequently border on blood channels (Fig. 6).


ORGA}IIZATION OF   A   LYMPH NODULE
                      ,a
    According to Peres--, henocytoblasLs 1n an ascidlan lynph nodule produce
lymphocytes which Lhen give rise to all other blood celL types,          I{emocytoblasts

are dlstinguished by the presence of a nucleolus.          The nucl-eus of the smaller,

less basophilic lynphocyte is reported to contaln, instead, patches of chromatLn.
Contrary to Peresr findings, electron nlcroscopy of a pharyngeal lynph nodule
from StgeJa cl.ava indicates that most differentiating        blood cells arise directly
from hemocytoblasts, not through a lynphocytic internediate.
    Henocytoblasts, the putative      DNA   synthesizing cel1s of autoradiograms, occur
in clusters in the center of a lynph nodule (tr'ig. 7); a few of these cells also
occur on the perlpheral marglns. Each group of hemocytoblasts is surrounded by
maturing blood ce11s in varlous stages of dlfferentlation.          Only a fev of lhe
perlpheral cells, which incLude phagocytes, compartment cells, and several types
of granular anoeboeytesl3, appear full-y matured; apparently most conpletely dif-
ferentiated cells are j-n circulating       b1ood. Connective tissue flbers surround       a


Fig. 1. Phase contrast light micrograph of a Ciona juvenile, six days after
         fertllization.  EN, endostyle; ES, esophagus; P, protostigrna;
       ' S, stomach. Bar in Figs. 1-6 equals 50 yn.

Tig. 2. Autoradiogram of longitudinal section through a Ciona juvenile shoning
        labeled hemocytobl-asts (arrows). P, protostigna; S, stomach.
Fig. 3. Autoradiograrn of longitudinal sectlon through transverse bar (TB)          and
        rms of stigna (ST) in pharynx of adult Ciona intestinaTis.
Fig. 4. Autoradiogram of henatogenic tissue in transverse bax of ciona showing
        labeled DNA syntheslzing ceJ-ls.
Flg. 5. Autoradiogram of cross section through body wa1l of stgela ciava showing
        l-abeled lyrrph nodules next to atrLal eplthel-lun (AE) and in connective
        tlssue. E, epldermlsl M, muscle.
I'ig. 6, Autoradlogram of lynph nodules belorr l-ntestlnal eplthellum of Pgura
         iaustor. Nodules border on blood channels (BC).
50



nodule and separate outLying blood cells from the pharyngeal epitheliun (Fig. 7).
     Hemocytoblasts border dlrectly   on one another, giving them angular outlines
(Tig. S).    They measure about 5 Um in dlameter and have a large, spherical

nucleus contalning one or trrro nucleoli and 1ittle    chromatin. A nucleolus nay
occur ln the center of a nucleus or adjacenL to the nuclear nembrane. Most cyto-
plasmic organelles cluster on one side of a cell.       This region contains several
round or oval mitochrondria and a small Golgi apparatus. A pair of centrioles
lies on the concave side of the Golgi clsterns, usually between the cisterns           and

the nucleus (Fig. 9).      Uost of the cytoplasn Ls fllled   with numerous polyribosomes
but a few clsterns of rough endoplasmic reticulum and an occaslonal srnall dense
granule (Flg. 8) are also present.
     DifferentLatlng leucocytes around the central hemocytoblasts lose their
prominent nucleolus as the amount of chronatin i.ncreases. Electron dense
granules usually appear in the cytoplasm, however, before lhe nuclear changes are
conpleted. As one procedes away from the center of a nodul-e, naturing blood
cells Lncrease in slze; their dense granules becone larger and more numerous.
Cel-l dLfferentlatlon    is also narked by the loss of polyribosones and the develop-
ment of elongate nltochondria, a larger Golgi apparatus, and long cisterns of

rough endoplasmic reticulum.

     Several i.Itrphocyte-like cell's (Ffg. f0) also occur ln the peripheral parts of
a nodule. They are similar to henocytoblaats in their cytoplasmic features, but
they are usually somelrhat smal1er, measuring about 4 }lltr' The nucleus lacks     a

consplcuous nucleolus, and patches. of chromatln occur al-ong the nuclear menbrane

and in the interior     of the nucleus. Sl-nce the nucl-eolus is apparently Lost
durlng cell division24, it is posslbte that some of these cel1s could be sten
ce11s which Just completed cell division.      Thls would account for Eheir snaller
eize ln a nodule.



Fig. 7. Electron micrograph of lyoph nodule in transverse bar froa pharyu of
        stgeTa cLava. C, connectlve tlssue fibers; GR, differentiatLng granular
        blood ce11s; II, henocytoblast; PE, pharyngeal epithellun.
52



DISCUSSION

     In prlnitive adult ascldiang,     hemopoietLc    tlssue occurs mainly in the
pharyngeal and gut rda1ls, This       distribution j-a 11ke that ln lower vertebrates
(e.g., lanpreys), where a deflnitive thynus and spleen are                         In   advanced
                                                                     "b".rrt25.
ascldians, hematogenic tissue is organized lnto distlnct nodules, where, as in
Stgela, a nodule is      composed   of one or two centers of divlding    hemocytoblasts

surrounded by non-dividlng, naturing blood          cell-s.   Lynph noduLes   lle within
connectlve tissue, either belolr bl-ood channels or epithella (pharyngeal,
epicardial, or atrial, but usually not digestive epithella). Those in the                  body

wall- of advanced specles probably followed the gonads as they nigrated anterlorly
from the gut loop. NoduLes could also have been lntroduced into the body wa1l by
way   of pharyngeal mesenterles.
     Ascldl-an blood   cells are a renewi-ng cel1 population     composed   of stem, translt-
iona1, and nature cells. They have a rapid late of proliferation which, at the
steady state, is bal"anced by the rate of ce1l loss. Since lnvertebrate chordates
are the.only deuterostomes nhose blood ce1ls are renewed, tt ts likel-y that the
phylogenlc orlgl-n of verteblate hemopoietlc tissue lles lrithin the Trnicata. In
echinoderns, blood cells have the characterlstics of expandirrg popr.r1"tioo"26,
that is, a stem cel-l     compartment whlch gives     rise to other blood cel1 types        does

not occur.    Sea   urchln amoebocytes have a slow rate of proliferation and show             a

slight increase in the percentage of labeled ceI1s with tLme;           some   cells which        do

not incorporate trLtiated thynldine possibly orlgl"nate from the parietal perito-
,r",-26. The starfish axlal organ,       Ttedmann    bodies, and other organs of the henal
systen which roere once considered to produce amoebocytes, are apparently not
specialized for henopoiesis2T.
     In stgela cJava,   bl-ood ce1ls are renewed    within several re.k"l0. By 20 days

Fig. 8. Section through henocytoblasts 1n center of nodule.             DG, dense granulel
           M, mitochondrion; Nu, nucleolus.
Flg. 9. Cytoplasnlc organelles Ln henocytoblast. CN, cmtrioles; G, Golgi
        cisterne; M, rnltochondrion; N, nucleusl PR, polytibosomes.
Fig. 10. Lynphocyte-like cell surrounded by dlfferentiating blood             ce11s.
il


after the LnJection of tritiated       thymidlne, cells in the perlpheral parts of           a

nodule ate now labeled.        Cel1s in the interior    of a nodule are no J-onger labeled;
presumabJ-y they have differentiated      into Eaturing blood ceL1s. By 60 days'         a

nodule as well- as most circulatlng      blood cells are no longer labeled.
     Blood cells in the periphery of a nodule are ln transitional         stages of dlf-

ferentlatlon.      Ful1y natured blood cells are apparently circulating       Lhroughout

the body. In other renewing populations of stgela c7ava, i.e,,            the gutl5    and

    -28
gonads-", where germinal and mature cel1s are easily distinguished because they
are spatially     separated, fully differentiated      cells do not proliferate.      It ls'
thus, probable that most fu1ly dlfferentiated          blood cells do not dlvide.      Vacuo-

lated ce1ls ln stge"la are not l-abeled at one hour but are labeled in both            J-ynph

nodules and circulatlng     blood after 20 d"ytl0.       kL Petophora annectens, compart-

ment cells and phagocytes but not other fu11y natured blood cells are reported

to be labeled by tritiated       thynldine29.
     Although sone differentiated     bLood ce11s can apParently divlde, nost DNA syn-

thesizing ceLLs are probably henocytoblasts. These cells, which also divide in
clrculating     blood, have a high nuclear-cytoplasnic ratio,      a Prominent nucleolus'
sparse chromatin, numerous polyribosomes, and few cytoplasmic organeJ-1es. These
features are also shared by undl-fferentlated geminal cells in Ehe ascidian gut
              30. As stem celJ-s, hemocytoblasts are capable of reproducing then-
eplthelirml4'
selves. as well as producing several- other cell types.         They are specl-allzed for

ce11 division as shown by the lncorporation of tritiated           thynldine lnto newly

synthesized DNA. The large nucleolus and abundant polyribosomes suggest'
respectively, active     RNA   and protein synthesis.     Polyribosomes are considered to

be sites for the synthesls of slructural- prot"its3l,         apparently to meet the
requirements of a rapidJ-y divlding cel1.
     Henocytoblasts in a juvenil,e and in an adult, although both stem cells,           can be

distingulshed by their kinetic behavior.         In a juvenile, nost ce1l prol"iferation
ls probably for the production of more hemocyLoblasts whereas that in an adult
is for the differentiation       of mature blood ceLls.
     Although the cell type that gives rise to all other ascidian bLood cells has
55



traditionally      been call-ed a lymphocyte, th18 terninology hae            led to confuslon
among   irnnunologists.        Based upon   vertebrate henatoLogy24, ascidian basophil-lc
blood ce1ls with a relatlvely J-arge nucJ-eus, prominent nucJ-eolus, and sparse
                                                                             13' 29
chromatin which have been referr<ld             to as 1)rmphocyt."ll' 12'        ^t" 'ot"
approprLately cal-Ied stem                      hemoblasLs22,   or hemocytoblasts. The sensi-
                                     ".11"32,
                                    33
tlvity of these cells to *-r"y"29'     i" characteristic shared by all relative-
                                          "
J-y undifferentiated cells of vertebrates, whether ln blood, dLgestive tfacta, or

gor.d"34. The role of ascidj-an bLood ce1ls in graft re3ection2, rosette forrna-
tion8, or the response to mitogensg is not well understood. !'urther studies
deflning the functlonal characterl-stlcs of the ascidian hemocytoblast shoul-d
therefore' contribute to our understanding of the phylogeny of the vertebrate
imtrune syatem.



ACIG'IOWLEDO.{ENTS

    part of thls research (a11 autoradiography and fixatlon of tissues for
el-ectron nlcroscopy) was conducted at the scripps Institution of oceanography'
La Jol-la, California. For support and guidance at this institution' I am grate-
ful- to Dr. Nicholas D. HolLand. For his suggestlons and many stimulati-ng
discussions, I thank Dr. Richard K. Wrlght. I am also grateful to Dr' Stephen S'
Rothman for suPPort during the preParation of this paper' The author is
presently a NIiI post-doctoral fellow at the University of Callfornla,                 San
Francisco.


REFERENCES

 I.     Berrill,     N. J.     (1955) The Origin of Vertebrates, oxford university Press,
        London.
 2. Reddy, A. L., Bryan, B. and Hildemann, W. H.                  (   1975) Immunogenetics 1 , 584-
        590.
  3.    Wright, R.      K.  4) J. Invertebr. Pathol . 24, 29-36 '
                              (Lg7

  4.    Wright, R.      K.                (1975) Amer . ZooL. 15 , 2I-27 '
                             and Cooper, E. L.
  5.    George, W. C. (1939) Quart. J. Mi-croscop. Sci. 81, 39L-428'
  6.    Mj-llar, R. H. (1953) L.M.B'C. Mem. Typ. Br. I"Iar. P1. Anim' 35'
  7.    GoodbodY, I.   (L974) Adv. Mar. Bio1. 12, 1-150.
  8.    Hildemannr W. H. and Reddy, A. L. (1973) Fed. Proc. 32, 2188-2194.
  9.    Hildemann, W. I{. and Uhlenbruck, G. (L974) in Progress in Immunology II'
        Vol. 2 (Brent , L. and Holborow, J., eds.), pp. 292-296, North-Holland'
        Ams   terdam.
56



10.   Emak, T. H. (f975) Experlenria 3f, 837-839.
11.   Kalk, M. (1963) Quart. J. llicroscop. Sci. 104, 483-493.
12. Overton, J. (1966) J. Morph. 119, 305-326.
13. Dudley, P. L. (1968) J. Morph. 124, 263-282.
14. Ernak, T. H, (1975) Ph.D, Dlssertation, University of California, San Dlego.
15. Ermak, T. H. (1975) J. Exp. ZooI. 194, 449-466.
16. Ermak, T. H. Ms. in preparatlon.
17. Tissues fixed ln 3% gJ-utaraldehyde in 0.1 M phosphate buffer with 0.7 U
    sucrose; postfixed ln lZ OsOO ln same buffered sucrose. SectLons examined
    on a JEM 1008 electron mi-croscope.
I8. Berrlll, N. J. (1936) Phi1. Trans. Roy. Soc. London 226, 43-70.                ,*t
                                                                                    -d

19. Millar, R. H. (1966) in Some Conremporary Studies in Marine Science
      (Barnes, H., ed.), pp. 519-534, Al1en and Unwin, Ltd., London.
20-   Berrill, N. J. (1950) The Tunicata, Ray Soclety, London,
2L.   Cowden, R. R. (1968) Trans. Amer. Mlcroscop. Soc. 87, 52I-524.
22.   Mukai, H. and Watanabe, H. (1976) J. Morph. I48, 337-362,
23.   Peres, J. M. (1943) Ann. Inst. Oceanogr, 2L, 229-359,
24.   Bessis, !1. (1973) Living Blood Ce1ls and Their Ultrastructure, Springer-
      Vgrlag, Heidelberg.
25. cood,.R. A., Finstad, J., Pol1ara, 8. and Gabrielsen, A. E, (1966) in
    Phylogeny of Imunlty (Soith, R. T,, Miescher, P. A. and Good, R. A., eds.),
    pp. 149-170, Universlty of Fl-orida Press, GaLnesville.
26. Ho1land, N. D. (1965) Biol. Bul"L. 128, 259-270.
27. tr'erguson, J. C. (1966) Trans. Amer. Microscop, Soc. 85, 2OO-209.
28. Errnak, T. H. (1976) Tiss. CelJ., in presa.
29. Freenan, G. (1970) J. Reticuloendothel. Soc. 7, 183-194.
30. Thonas, N. !L (1970) J. Mar. Biol. Ass. U.K. 50, 737-746.
31. Palade, G. (1975) Science f89, 347-358.
32. Snith, M. J. (1970) Bio1. 3u11. 138, 354-378.
33. Freenan, c. (1964) J. Exp. Zoo7. 156, 157-184.
34. Patt, H. M. and Quastler, H. (1963) Physiol. Rev. 43, 357-396.


                                                                                   I

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Phylogeny of Thymus and Bone Marrow Cells

  • 1. Phylogeny of Thymus and Bone Marrow - Bursa Cells, R.K. Wright and E.L. Cooper eds. @ Elsevier/North-Holland Biomedical Press, Amsterdam, The Netherlands THE IIEUATOGENIC TISSUES OF TIJNICATES Thomas H. Ernak . DepartmenL of Physlology Unlver.sltY of Callfornia !tredical Center San Fiancisco, Cal-lfornla 94143 INTRODUCTIOTiI Tunlcates are unique among lnvertebrates in that they share such chordaLe characterl-stics as a notochord, dorsal tubul-ar nerve cord, and pharyngeal- gill slits with the vertebrates. The ascidlans, a group of sessile tmicates' are generally considered to have glven rLse Lo the vertebrates via a pelaglc tadpole latval. feeding mrlne RecenLly, biol-ogists have turned toward these fllter 3' 4' animals 1n an attempt to understand the origin of the lunune t""pot"t2' Speclal- attention has focused on the ascidian lynphocyte, a relatively undiffer- entiated cell that l-s comon to all ascldian species and generates all other 6'7. circulatlng lF'phocytes are reported to participate ln blood ce1l ayp."5, the rejectlon of allografts2, fot rosettes wlth sheep red blood cells8, and respond to phytohenagglutinlng. ByautoradiograPhywlthtrltiatedthyflidine,bloodcel].sengagedlnPremitotic DNA synthesis have been localized Ln the tlssue s of Stgela "7"n"IO. Ascidian bl-ood cells, which constitute a renewing ceL1 populatlon' proliferate in clrcu- lating blood and in lyaph nodules throughout the body' The ultrastructure of 12' 13 b.a toa several- types of bl-ood celLs has been described in blood "p".."ll' in a lynph nodule. For thLs study, a postlarval ascldian Juvenile and several 15' 16 for a short time adul-t ascldians were exposed to tritlated thyrnldinel4' l-nterval in order to localize sites of hematoge[ic activlty. In StgeTa clava, the organlzation of a pharyngeal Lymph nodul"e was exanined by electron micros- copy" the putative DNA synthesizing ce1ls described' "nd HEMATOGENESIS IN A POSTLARVAL JUVENILE The Ciona intestinalis juvenile (Fig. 1) is considered to most closely 45
  • 2. 6 i' L9 resemble the ancestral ascidi-"rr18' and is essentially a sirnpltf ied adult. Af ter metamorphosis, it has a beati-ng heart , a si-ngle incurrent siphon, two widely spaced excurrent siphons, and a pair of primitive gill slits (protostig- mata) on each side of the ph"ryrr*2o. The gut loop lies slightly behind and to the left of the pharynx. Numerous hemocytoblasts, undlfferentiated ce1ls hrith a large, nucl"eolated nucleus and little basophil-lc cytoplasm, and a few presmbly differentiated ce11s cluster in the pharyngeal wall around the protostigmata and near the endostyle. Hemocytoblasts originate fron cel1s of the archent..or2l and are especlalLy numerous below germinal cells in the stignatlc eplthellul[. Clusters of these prinitive blood celLs do not occur around the postpharyngeal gut. In autoradio- grams, hemocytoblasts are labeled with tritlated thymidine (fig. 2). With continued dlvislon and by nlgratlon, the pharyngeal hemocytoblasts w111 give rise to henatogenLc tissue in the pharynx and around the gut of an adult Cjona. They will probably also suppty gerninal cel-Is for the ovary and testis22. DISTRIBUTION OI' I{EMATOGENIC SITES IN ADIJI,T ASCIDIANS In adult ascidians, the pharynx is a greatly enlarged organ perforated by a multltude of ciliated gill s11ts (stigmata). HemaLogenlc tissue occurs 1n the pharyngeal wa1l, around the di-gestive tract, and anong advanced solitary species, ln the body walI, Each ascidian fanlly exhiblts a characteristic relationshlp befween pharynx, postpharyogeal gut (esophagus, stomach, and intestlne), and gonads, and the distrLbution of henatogenic tlssue foLlows accordingly. An adult Ciona intestinal.is has several of the most prinltlve ascidian body features. The postpharyngeal gut lies slightly behind the pharlmx, and the gonads f-ie withln the curvature of the dlgestive tract. Hematogenic tissue ls abundant in the pharyngeal wa1l and around the gut-l-oop. A few clueters also occur in the body lralf at the posterlor end of the body6 and where the pharynx i.s attached to the body wa11, either under the endostyle or by mesenteries. Except in these reglons, blood formlng tissue is absent from the body wa11. Henatogenic cel-le Ln the pharynx of Ciona are abundant ln transverse bars
  • 3. 47 (Flg. 3) and scattered in longitudinal bars and al-ong the endostyle. Blood cells are arranged 1n smalJ-, diffuse clusters adjacent to the pharyngeal ePitheliun; ce11s labeled vlth trirlated thymidine are scattered throughout the tissue (Fig. 4). Most non-dividing cel1s are presumed to be Partially or fu1ly differentiated blood cells. Around the gut, hematogenic tj-ssue is aLso diffuse and associated wlth connectlve tissue or the external gut linlng. Clustered blood cells may be so plentiful as to 1ie cLose to the stomach ePltheliun. In regions rthere the gonads are present, hemaEogenic tissue is sparse. Ta cheTgosona productum and Ascidia ceratodes, other solltaly ascidians whose gonads lie within the gut LooP' most hemtogenic tissue ls around the gut and organized into sna1l nodules containing several cel-ls whlch incorPorate tritiated thynidlne. Lynph nodules are assoclated with connective tissue and blood chan- nels but not the external or internal gut eplthelial nodules also frequently occur near the gonade. The gut-loop of most colonial ascldlans is U-shaped and lies behind the pharyu, a delLcate structure contalning lLtt1e hernatogenlc tissue. In PoTgcTinum p-lanum and Euherd.nania cTavitotmis, clusters of labeled blood celLs are most abundant in the region of the gut-loop where they occur Ln small Patches ln the connective tlssue and adjacent to the eplcardium, a singl,e pouch alongsLde the gut but not llning it. The gonads of advanced sPecles 1le withln the body wall' and it Ls only ln these specles that lynph nodules are abundant ln this regl-on. In StgeJ.a c-Zava' nost lynph nodules occur 1n the pharyngeal and body walls; few occur around the .10 postpharyngeal gut--. Although no nodules have bee4 observed below the stomach eplthellurn, a ferr scattered ones are seen in the connectlve tissue around the intestinal epitheliun. Lymph nodules 1n the body wall l"le next to the atrial epithelLum and in the connectlve tissue linlng blood channels (Fig. 5)' Some nodules also occur in the endocarps, projections of the atrial epltheliun filled with connective tissue and blood cells. In Stye-la, a nodule conslsts of one or two groups of ce1ls Labeled wlth trltiated thynidine surrounded by several un- labeled ce11s. Many of the DNA syntheslzing ceLl-s are hemocytoblasts with a
  • 4. 4 dj-sLinct nucleolus. In lftolgufa verrucifera and Pguza haustot, where both the gut and gonads lie withl-n the body wa1l, distlnct l,ynph nodules occur both in the connectlve tlssue and adjacent to the atrlal epitheLLun. In the connective tissue, nodules frequently border on blood channels (Fig. 6). ORGA}IIZATION OF A LYMPH NODULE ,a According to Peres--, henocytoblasLs 1n an ascidlan lynph nodule produce lymphocytes which Lhen give rise to all other blood celL types, I{emocytoblasts are dlstinguished by the presence of a nucleolus. The nucl-eus of the smaller, less basophilic lynphocyte is reported to contaln, instead, patches of chromatLn. Contrary to Peresr findings, electron nlcroscopy of a pharyngeal lynph nodule from StgeJa cl.ava indicates that most differentiating blood cells arise directly from hemocytoblasts, not through a lynphocytic internediate. Henocytoblasts, the putative DNA synthesizing cel1s of autoradiograms, occur in clusters in the center of a lynph nodule (tr'ig. 7); a few of these cells also occur on the perlpheral marglns. Each group of hemocytoblasts is surrounded by maturing blood ce11s in varlous stages of dlfferentlation. Only a fev of lhe perlpheral cells, which incLude phagocytes, compartment cells, and several types of granular anoeboeytesl3, appear full-y matured; apparently most conpletely dif- ferentiated cells are j-n circulating b1ood. Connective tissue flbers surround a Fig. 1. Phase contrast light micrograph of a Ciona juvenile, six days after fertllization. EN, endostyle; ES, esophagus; P, protostigrna; ' S, stomach. Bar in Figs. 1-6 equals 50 yn. Tig. 2. Autoradiogram of longitudinal section through a Ciona juvenile shoning labeled hemocytobl-asts (arrows). P, protostigna; S, stomach. Fig. 3. Autoradiograrn of longitudinal sectlon through transverse bar (TB) and rms of stigna (ST) in pharynx of adult Ciona intestinaTis. Fig. 4. Autoradiogram of henatogenic tissue in transverse bax of ciona showing labeled DNA syntheslzing ceJ-ls. Flg. 5. Autoradiogram of cross section through body wa1l of stgela ciava showing l-abeled lyrrph nodules next to atrLal eplthel-lun (AE) and in connective tlssue. E, epldermlsl M, muscle. I'ig. 6, Autoradlogram of lynph nodules belorr l-ntestlnal eplthellum of Pgura iaustor. Nodules border on blood channels (BC).
  • 5.
  • 6. 50 nodule and separate outLying blood cells from the pharyngeal epitheliun (Fig. 7). Hemocytoblasts border dlrectly on one another, giving them angular outlines (Tig. S). They measure about 5 Um in dlameter and have a large, spherical nucleus contalning one or trrro nucleoli and 1ittle chromatin. A nucleolus nay occur ln the center of a nucleus or adjacenL to the nuclear nembrane. Most cyto- plasmic organelles cluster on one side of a cell. This region contains several round or oval mitochrondria and a small Golgi apparatus. A pair of centrioles lies on the concave side of the Golgi clsterns, usually between the cisterns and the nucleus (Fig. 9). Uost of the cytoplasn Ls fllled with numerous polyribosomes but a few clsterns of rough endoplasmic reticulum and an occaslonal srnall dense granule (Flg. 8) are also present. DifferentLatlng leucocytes around the central hemocytoblasts lose their prominent nucleolus as the amount of chronatin i.ncreases. Electron dense granules usually appear in the cytoplasm, however, before lhe nuclear changes are conpleted. As one procedes away from the center of a nodul-e, naturing blood cells Lncrease in slze; their dense granules becone larger and more numerous. Cel-l dLfferentlatlon is also narked by the loss of polyribosones and the develop- ment of elongate nltochondria, a larger Golgi apparatus, and long cisterns of rough endoplasmic reticulum. Several i.Itrphocyte-like cell's (Ffg. f0) also occur ln the peripheral parts of a nodule. They are similar to henocytoblaats in their cytoplasmic features, but they are usually somelrhat smal1er, measuring about 4 }lltr' The nucleus lacks a consplcuous nucleolus, and patches. of chromatln occur al-ong the nuclear menbrane and in the interior of the nucleus. Sl-nce the nucl-eolus is apparently Lost durlng cell division24, it is posslbte that some of these cel1s could be sten ce11s which Just completed cell division. Thls would account for Eheir snaller eize ln a nodule. Fig. 7. Electron micrograph of lyoph nodule in transverse bar froa pharyu of stgeTa cLava. C, connectlve tlssue fibers; GR, differentiatLng granular blood ce11s; II, henocytoblast; PE, pharyngeal epithellun.
  • 7.
  • 8. 52 DISCUSSION In prlnitive adult ascldiang, hemopoietLc tlssue occurs mainly in the pharyngeal and gut rda1ls, This distribution j-a 11ke that ln lower vertebrates (e.g., lanpreys), where a deflnitive thynus and spleen are In advanced "b".rrt25. ascldians, hematogenic tissue is organized lnto distlnct nodules, where, as in Stgela, a nodule is composed of one or two centers of divlding hemocytoblasts surrounded by non-dividlng, naturing blood cell-s. Lynph noduLes lle within connectlve tissue, either belolr bl-ood channels or epithella (pharyngeal, epicardial, or atrial, but usually not digestive epithella). Those in the body wall- of advanced specles probably followed the gonads as they nigrated anterlorly from the gut loop. NoduLes could also have been lntroduced into the body wa1l by way of pharyngeal mesenterles. Ascldl-an blood cells are a renewi-ng cel1 population composed of stem, translt- iona1, and nature cells. They have a rapid late of proliferation which, at the steady state, is bal"anced by the rate of ce1l loss. Since lnvertebrate chordates are the.only deuterostomes nhose blood ce1ls are renewed, tt ts likel-y that the phylogenlc orlgl-n of verteblate hemopoietlc tissue lles lrithin the Trnicata. In echinoderns, blood cells have the characterlstics of expandirrg popr.r1"tioo"26, that is, a stem cel-l compartment whlch gives rise to other blood cel1 types does not occur. Sea urchln amoebocytes have a slow rate of proliferation and show a slight increase in the percentage of labeled ceI1s with tLme; some cells which do not incorporate trLtiated thynldine possibly orlgl"nate from the parietal perito- ,r",-26. The starfish axlal organ, Ttedmann bodies, and other organs of the henal systen which roere once considered to produce amoebocytes, are apparently not specialized for henopoiesis2T. In stgela cJava, bl-ood ce1ls are renewed within several re.k"l0. By 20 days Fig. 8. Section through henocytoblasts 1n center of nodule. DG, dense granulel M, mitochondrion; Nu, nucleolus. Flg. 9. Cytoplasnlc organelles Ln henocytoblast. CN, cmtrioles; G, Golgi cisterne; M, rnltochondrion; N, nucleusl PR, polytibosomes. Fig. 10. Lynphocyte-like cell surrounded by dlfferentiating blood ce11s.
  • 9.
  • 10. il after the LnJection of tritiated thymidlne, cells in the perlpheral parts of a nodule ate now labeled. Cel1s in the interior of a nodule are no J-onger labeled; presumabJ-y they have differentiated into Eaturing blood ceL1s. By 60 days' a nodule as well- as most circulatlng blood cells are no longer labeled. Blood cells in the periphery of a nodule are ln transitional stages of dlf- ferentlatlon. Ful1y natured blood cells are apparently circulating Lhroughout the body. In other renewing populations of stgela c7ava, i.e,, the gutl5 and -28 gonads-", where germinal and mature cel1s are easily distinguished because they are spatially separated, fully differentiated cells do not proliferate. It ls' thus, probable that most fu1ly dlfferentiated blood cells do not dlvide. Vacuo- lated ce1ls ln stge"la are not l-abeled at one hour but are labeled in both J-ynph nodules and circulatlng blood after 20 d"ytl0. kL Petophora annectens, compart- ment cells and phagocytes but not other fu11y natured blood cells are reported to be labeled by tritiated thynldine29. Although sone differentiated bLood ce11s can apParently divlde, nost DNA syn- thesizing ceLLs are probably henocytoblasts. These cells, which also divide in clrculating blood, have a high nuclear-cytoplasnic ratio, a Prominent nucleolus' sparse chromatin, numerous polyribosomes, and few cytoplasmic organeJ-1es. These features are also shared by undl-fferentlated geminal cells in Ehe ascidian gut 30. As stem celJ-s, hemocytoblasts are capable of reproducing then- eplthelirml4' selves. as well as producing several- other cell types. They are specl-allzed for ce11 division as shown by the lncorporation of tritiated thynldine lnto newly synthesized DNA. The large nucleolus and abundant polyribosomes suggest' respectively, active RNA and protein synthesis. Polyribosomes are considered to be sites for the synthesls of slructural- prot"its3l, apparently to meet the requirements of a rapidJ-y divlding cel1. Henocytoblasts in a juvenil,e and in an adult, although both stem cells, can be distingulshed by their kinetic behavior. In a juvenile, nost ce1l prol"iferation ls probably for the production of more hemocyLoblasts whereas that in an adult is for the differentiation of mature blood ceLls. Although the cell type that gives rise to all other ascidian bLood cells has
  • 11. 55 traditionally been call-ed a lymphocyte, th18 terninology hae led to confuslon among irnnunologists. Based upon vertebrate henatoLogy24, ascidian basophil-lc blood ce1ls with a relatlvely J-arge nucJ-eus, prominent nucJ-eolus, and sparse 13' 29 chromatin which have been referr<ld to as 1)rmphocyt."ll' 12' ^t" 'ot" approprLately cal-Ied stem hemoblasLs22, or hemocytoblasts. The sensi- ".11"32, 33 tlvity of these cells to *-r"y"29' i" characteristic shared by all relative- " J-y undifferentiated cells of vertebrates, whether ln blood, dLgestive tfacta, or gor.d"34. The role of ascidj-an bLood ce1ls in graft re3ection2, rosette forrna- tion8, or the response to mitogensg is not well understood. !'urther studies deflning the functlonal characterl-stlcs of the ascidian hemocytoblast shoul-d therefore' contribute to our understanding of the phylogeny of the vertebrate imtrune syatem. ACIG'IOWLEDO.{ENTS part of thls research (a11 autoradiography and fixatlon of tissues for el-ectron nlcroscopy) was conducted at the scripps Institution of oceanography' La Jol-la, California. For support and guidance at this institution' I am grate- ful- to Dr. Nicholas D. HolLand. For his suggestlons and many stimulati-ng discussions, I thank Dr. Richard K. Wrlght. I am also grateful to Dr' Stephen S' Rothman for suPPort during the preParation of this paper' The author is presently a NIiI post-doctoral fellow at the University of Callfornla, San Francisco. REFERENCES I. Berrill, N. J. (1955) The Origin of Vertebrates, oxford university Press, London. 2. Reddy, A. L., Bryan, B. and Hildemann, W. H. ( 1975) Immunogenetics 1 , 584- 590. 3. Wright, R. K. 4) J. Invertebr. Pathol . 24, 29-36 ' (Lg7 4. Wright, R. K. (1975) Amer . ZooL. 15 , 2I-27 ' and Cooper, E. L. 5. George, W. C. (1939) Quart. J. Mi-croscop. Sci. 81, 39L-428' 6. Mj-llar, R. H. (1953) L.M.B'C. Mem. Typ. Br. I"Iar. P1. Anim' 35' 7. GoodbodY, I. (L974) Adv. Mar. Bio1. 12, 1-150. 8. Hildemannr W. H. and Reddy, A. L. (1973) Fed. Proc. 32, 2188-2194. 9. Hildemann, W. I{. and Uhlenbruck, G. (L974) in Progress in Immunology II' Vol. 2 (Brent , L. and Holborow, J., eds.), pp. 292-296, North-Holland' Ams terdam.
  • 12. 56 10. Emak, T. H. (f975) Experlenria 3f, 837-839. 11. Kalk, M. (1963) Quart. J. llicroscop. Sci. 104, 483-493. 12. Overton, J. (1966) J. Morph. 119, 305-326. 13. Dudley, P. L. (1968) J. Morph. 124, 263-282. 14. Ernak, T. H, (1975) Ph.D, Dlssertation, University of California, San Dlego. 15. Ermak, T. H. (1975) J. Exp. ZooI. 194, 449-466. 16. Ermak, T. H. Ms. in preparatlon. 17. Tissues fixed ln 3% gJ-utaraldehyde in 0.1 M phosphate buffer with 0.7 U sucrose; postfixed ln lZ OsOO ln same buffered sucrose. SectLons examined on a JEM 1008 electron mi-croscope. I8. Berrlll, N. J. (1936) Phi1. Trans. Roy. Soc. London 226, 43-70. ,*t -d 19. Millar, R. H. (1966) in Some Conremporary Studies in Marine Science (Barnes, H., ed.), pp. 519-534, Al1en and Unwin, Ltd., London. 20- Berrill, N. J. (1950) The Tunicata, Ray Soclety, London, 2L. Cowden, R. R. (1968) Trans. Amer. Mlcroscop. Soc. 87, 52I-524. 22. Mukai, H. and Watanabe, H. (1976) J. Morph. I48, 337-362, 23. Peres, J. M. (1943) Ann. Inst. Oceanogr, 2L, 229-359, 24. Bessis, !1. (1973) Living Blood Ce1ls and Their Ultrastructure, Springer- Vgrlag, Heidelberg. 25. cood,.R. A., Finstad, J., Pol1ara, 8. and Gabrielsen, A. E, (1966) in Phylogeny of Imunlty (Soith, R. T,, Miescher, P. A. and Good, R. A., eds.), pp. 149-170, Universlty of Fl-orida Press, GaLnesville. 26. Ho1land, N. D. (1965) Biol. Bul"L. 128, 259-270. 27. tr'erguson, J. C. (1966) Trans. Amer. Microscop, Soc. 85, 2OO-209. 28. Errnak, T. H. (1976) Tiss. CelJ., in presa. 29. Freenan, G. (1970) J. Reticuloendothel. Soc. 7, 183-194. 30. Thonas, N. !L (1970) J. Mar. Biol. Ass. U.K. 50, 737-746. 31. Palade, G. (1975) Science f89, 347-358. 32. Snith, M. J. (1970) Bio1. 3u11. 138, 354-378. 33. Freenan, c. (1964) J. Exp. Zoo7. 156, 157-184. 34. Patt, H. M. and Quastler, H. (1963) Physiol. Rev. 43, 357-396. I