Cellular and Histological Aspects of Developing Porcine Adipose Tissue
CELLULAR AND HISTOLOGICAL ASPECTS OF DEVELOPING PORCINE A DIPOS€ nssw
by Gary J. Hausman’“
INTRODUCTION gi owing adipocyte, the devcblopment of thclse r,lc- ments is paramount to adipocytc hypertrophy. An Adipose ti\\iic may seem to be a most unexciting understanding of the stromal-vascular development and simple tissuc fiom a histological standpoint. The of adipose tissue is essential to the complete undcr- \im and high lipid content of unilocular adipocytes standing of adipocyte hyperplasia and hypertrophy. make\ adiposc tissue extremely hard to study with \tdndard histological techniques. However, before Presumptive ad;pose tissue of pigs (Hausman and cutcmive adipocyte hypertrophy occurs, adipose KauEman, 1978), calves (Bell, lW), and lambs tis\ue is a very dynamic and organized tissue and can ( Wensvoort, 1967) is a lipid-free bed of short, 2111- 1)~studied I~istologicallywith relative ease. organized collagen fibers in which cclls of various Adipose, tissue histogenesis is extremely important shapes and sizes arc situated (Figure 1).Gradually, to thc red meat industry since it is the first step these fibers become better organized and eventually ~iivolvc.rI in the annual production of 12 billion form complete connective tissue ( C.T. ) borders poiind5 of fat by American farmers. Only through a around small developing fat cell clustcm (Figure 2, complc+c. untlc.rstanding of adipose tissue formation A). Many patterns of connective tissue organization cm \v(> ever attcmpt to control its devclopment. The cvist between a common origin and destiny for brown vic.w\ on adipose histogenesis that are taught in and white adipose tissue (WAT) of many spccies niodcrn histology texts were developed during the (Figure 3). Since the connective tissue of BAT of most latch 1800’s. Sincc that time until now, this is an area species is very organized before cellular lipid depo- of literature which is extremely confusing and con- sition begins, it is considered developmentally dis- tioversid. Thcb early work was confounded by species tinct from WAT. For all WAT and even some BAT and amtomica1 \it<. variation and by the presence of ( sheep ) lipid deposition occurs before complctc C.T. 1)iown adipose ti5\uc (RAT) in a number of species borders are formed. In every casc, thcy arc cvcwtii- \tudic d. Also, \om(’ workers, past (Flemming, 1871) ally formed before they approach the stilt(, of th(1 and prcvnt ( Napolitano, 1963 ), were concerned pri- mature WAT lobule ( Figurc 3). marily with histogenesis at thc individual cell level Presumptive adipose space of meat animals is .i~itl did not considcr the tissuc aspects. I mention space that by C.T. definition will eventually be filled thrsc~two tvorkcm in particular because their work w:th adipocytes. It contains very delicate strands of 112s had profound influclncc on shaping our commonly C.T. fibrrs and has few, irregularly shaped cells other IK Id views on adiposc tissue histogenesis. than fat cells (Figure 2). \\’hilc~ adipocytes arc \f7ith the advent of the elcctron microscope and “filling” this space, the C.T. border becomes thicker rc+incd techniqnc~\, tnorc recent work has provided arid more compact ( Figui L‘ 4,A,B ). Thc C.T. attains vc’iy accuratc invght into adipow tissue formation. a maximum thickness when the “space” is filled with Thc hulk ot this mork ha\ bcwi conductcld on meat adipccytes. The connective tissue then becomes ani!nals, while in the c.ise of the Ic1b animals, little ively thinner with further hypc,rtrophy of advmccment has hecn made. De5pite the advances the adipocytes ( Figure 4,C ). T~LIS,the stromal de- that liavc. bcwi made, a imifying concept of adipose velopment of adipose tissuc is only affected by “adi- ti5\uc, devc.lopment is still nonexistent. In this review, pocytc dcvelopmcmt” after thc presumptive adiposc, I will dcmonstratc devc~lopmcntalconcepts of adiposc space is “fillcd .” IVha t controls t hc. stromal dcvel op- ti\\w which propow a common origin and common tl(~~tiiiyfor ,111 adipo.c tissue. Sircimal-S’asciil~ir DewIopment. The diffuse and “G. J. IIAC!SMAN extensive nature. of adipose tiww may obscure thc fact that adiposc tissue possesses organized stromal- Post Doctorul Scliolur, Dniy and An final Science vascular components. Since the stromal-vascular ele- Depurtment, The Pennsylouniu State Cinicrisity, ments providc \tnicture and slipply nutrients for the CTiLicerPitij P~irk,Pennsy1z;ania 16802
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FIGURE 1. Fetal porcine dorsal subcutaneous tissLie stained with the Lillie’s Allo- chrome stain !collagen) (A, X 1400) and Harris Hematoxylin and Eosin (6, X 875).
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FIGURE 2. Presumptive (porcine) adipose space demarcated by o complete connective tissue border (arrows), stained with the Lillie’s Allochrome stoin (collagen) (A) and Harris Hematoxylin ond Eosin (B), X 875. Note the delicate stronds of C.T. fibers ond few irregularly shoped cells surrounding the central fat cell clusters.
with relatiwly thick adventitial la) ers in bovine adi- and packing of branched. basophilic cclls into sev- pose (Bell, 1909) or as several “cuffs” of cells rmged eral l‘iyers of “cuffs” of similarly oriented cells (Fig- around capillaries in porcine ( Herman$, 1973) and lire 6). Presumptive adipow lobules are the source of ovine ( Wensvoort, 1967) adipore tis5ue. We ha\e adipocytcs and capillaries of developing fat cell dcxxibed the formation of presumptive adipose lob- clustcm (Figure 7). The cells of the presumptive ules in porcine adiposc tissiic (Figure 6). The pre- lobules either lwcomc adipocytes or the endothelial sumptivc lobules were formed by the condensation cells of thc. capillary walh.
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Sinal1 unilocular cells and multilocnlar cells havc PRESUMPTIVE ADIPOSE TISSUE I)cwi observed continiiously in postnatal pig adipotcb (hlc.rsmann et n7, 1975), up to and including 150 days of age. ORGAN TION The literaturc contains much c~idcncrfor an cndo- thelia1 or reticular-endothelial origin for hrown and BAT, rat, rabbit, cat white adipocytes. \hny studics have indicated a close dcwclopmental relation5hip betwclen adipocytes and ORGANIZATION CELLULAR LIPID blood vessels ( Flcmming, 1871, Toldt, 187’0; Rmvicr, RESULTING IN / DEPOSITION BEGINS A COMPLETE 1875; Pollakoff, 1888, \l’assc.rinann, 1965, Barnard, CONNECTIVE 1F69; Kapolitano, 1963; Sheldon, 1969; Naplitano aid TISSUE BORDER BAT, sheep Fawcett, 1955, Simon, 1965; Imaeda, 1959; I)esiioyc.rs AROUND A GROUP OR GROUPS OF and Vodovar, 1974; Bell, 1909 ). Adipogenesis was ADIPOCYTES WAT, cattle bound to proliferation of blood vessclls in subcutanc- LIS tissue (Simon. 1965, Flcmming, 1871 ), and iii thc F WAT, pig, human mouse epididymal fat pad (Wassermann, 1965). In sheep ( \Vc.nsvoort, 19671, pig ( Hermans, 1973), hu- man and rat (Simon, 1965) adipose tissue, perivas- MATUl ION cular reticulum cells were considcred “~~r~~adipocytcs.” \Vasscnnann’$ ( 1965) primitive fat organs of man were‘ formed by the giowth of both the c.ndothvlia1 and adventitial ccllt of thick blood \~eswls. Early st1idir.s demonstrated the upt‘tkr of A piticnlatc. dye FIGURE 3. Relative onset of formation of a complete con- by matiii c adipow cells ( Bremcr, 1937‘; Dogliotti, nective tissue border around group(s) of adipo- cytes in relation to cellular lipid deposition. 1hB; McCollough, 1914), fat cell\ depleted of lipid (Dogliotti, 1928; Latta and Rutledge, 1935 ), and immature fat cells ( Chang. 1940; McCollough, 1944). A number of earlier investigators (Lowc, 1878; Ehr- Many p‘ittcwis of adipose lobule formation exist man, 1883; Gag<., 1882; \\’adeyer, 1875; Rohritiky, Ii(~t\w~wa comnion origin ( presumptive adipose lob- 1885; Voljakoff, 1888) believed that in sonic’ c‘ist‘b ule) md tlcstmy (mature WAT lobule) for adipose fat cells wcrc derived from “wandering cells” of con- tis5iie (Figiirc 8). In every case. adipose lobules are nective tistuca. PoljaLoff (1888) and RobritLky (1885) f 01 mcd, c~~cnthough lohule formation may seem less indicated that fat cells coriltl revert back to wandrr- “tpeci,ili/cd” or organized in yome cases since it oc- mg cells in certain caws. Ft’arthin ( 1903 ) dcxribed cur$ after lipid deposition has begun. In every in- the transformation of adipose to lymphoid tissue as stance, it is an identical process that leads to the same being initkted by dilation of blood capillaries, re- prodiict ( matarc) \VAT lobule), The only variable is moval of lipid from the adipose cclls along the dilatcd the tmc at which cellular lipid deposition begins capillaries, followed by eonvcrsion of thew ccllt into (Figure 8). reticular cells and thcm the growth of lymphoid elc>- F‘it cell cliistri s bccome larger due to hypertrophy nients into the meshcs of the rcticulum. More rcwntly ;tnd hyperplasia of lipid droplc~tswhich spreads out Dcsnoyers et NZ. (1974) looked at thc fetal dc~c1lop- the origin~lprc,sumptive adipose lobule ( Figure 9). ment of pericardial and epididymal adiposc titsuc of Tlicsr “multilo~iilar” adipocytes become unilocular the p’g. Tl-.eir ultrastructur,il study of lipid-frw cellt throiigh the coalrwence of inany lipid droplets into u~idvery primitive ac1ipocyte.s suggested to thcm A oi~~Iciig(>droplclt (Figure 9,Il ). In bovine cidiposc~, perivasciilar origin for thc aclipocytc,. Thry considered this matiiration proc is complc~tcat birth (Jenkin- frw endothcljal cell5 as prcadipocyt( t and found thc \on et al , 1968 ), while in the pig, it only begins after i3itcXnsity of proliferation of preadopocytes closel) hirth (hlersmann et al, 1975) In heep thi$ conver- rc,latc,d to thcl formation of new 11lood capillaries. In sion occurs 2-3 wcc~ks after birth (Grmniel et ul., our study 011 dcvcloping pig subcutancout, wv li~vc~ 1970) and represents a transition of BAT to \\.AT as suggrsted an entlothelial origin for pig ac1ipocytc.s as widcnccd by elc~tron microscopic observations \vel 1. \\’e found the morphc )I ogi cal char acter i s t i cs of (Gemmc.1 et al., 1970) In nine-day and older pigs, thc. cwliclst ,iclipocytc\ to hc very similar to cndo- multil!)ciilcir adipocytcs w(w found singly or in small thr Iial cr.11~ ( Figurc 11). Thc simultaneous appcw- groiipt within rinilociilar fat cc~llIobul(~~ ( Figurc 10). ance of early ad;pocytc>t and L,ipillaries WPI c hirtlicr
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FIGURE 6. Fluorescence of RNA and RNA in a fresh frozei section of fetal dsrsal sutcutaneous tissue with acridine orange staining. The DNA in nuclei appears as the bright material whilz cytoplasmic RNA appears as the dull material. Several presumptive adipose lobules are present as well as the apparent formation of a presumptive lobule due to alignment and packing of surrounding cells (arrows) X 325.
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F- FIGURE 7. The concept of !he presumptive odipo:e lobule. Fresh frozen sections (30 u) of the inner layer of dorsal subcutaneous tissue of on area cranial and dorsol to the first rib. A, B, D, and F are sections stained with Oil Red 0 and Horris hematoxylin, while C, E, and G are sections from Pelikaq dye injected fetuses counterstoined with Harris hemotoxylln. Sections ore from 45 d3y fetuses (A), 60 day fetuses (B,C), 75 day fetuses (D,E) and 105 day fetuses (F,G). Note the presumptive adipose lobules (pc) ore closely related to the capillaries (c) and odipocytes (a) of the developing adipose lobules (1). X 110.
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hetc~rologour hem,itopoic+s occiiircd commonly in adipose tissuc. 1Ic al4o rcprtcd tlr,it adipose tiwic bccamc. thc soiircc of abundant Iymphadconoid tissric chiri 11g ad r cwa1 in s u ffi c i cn cy, 11 11dc r con d i t io t 1 s ( f s t rc 5 4 and following splencctomy. Hollcnberg ct (11. ( 1970) rchportcd that small islands of lymphoid tissiie wvre frcyiently observed in histological preparations of WAT, human adiposrx tissue. In dcvcloping porcine adipose tissric, we have observed the full range of cells common to rcd honc. marrow in fetal and c,.irly postnatal animals DEPOSITION BEGINS ( Figure 12). These report4 intlicatc, that adipose ti\- siic' may histogenetically rclatcd to ti\\iies such 'is BAT, sheep lw Iwne marrow and lymph nodc~.Factois that control thc ,tccrimulation of lipid in adipose tissue, might 11o similar to factors that control thv convc~sionof- ret1 to ycllow hone niarrow and the irivolutio~iof Iyrnpli nodes with lipid.
~ WAT MATURE LOBULE Deoelnpmentul Grcrtlients. 1I7c have dcwrilwd ( Hausman and Kauffman, 1978 ) various devclop- nicntal gradients in frtal poi cine subcutaneous adi- !~rhule Formation = the resolution of the presumptive adipose lobules into a number of capillaries and pose tissiic. At all fetal stages, the C.T. stroma wci\ associated adipocytes. Development occurs more dcfincd antl lwttcr organi/d ;is thc. scwtions so that capillaries are surrounded by only one layer of adipocytes. l)ecamc> more cCiiiclJ anatomically. This caudcil to ~'1s FIGURE 8. Relotive onset of odipose lobule formotion in re- cranial grdicvit for stromal dcvc.lopinont prcscvit lation to cellulor lipid deposition. in 43-day fetuscs, although no lipid or apparcwt tat cells were present at this time (Figure 13). A grad- icnt of stromal clcvelopmcwt from ventral to dorsal in sripport for this contention. Ultrastructiiral ( Rarnarcl, sulmitaneoas adipose. was alw obscrvcd throughoiit 1969; Kapolitano ai~lFawcvtt, 19.58 ) and mitotic fctal drvcloptmcnt ( Figure 4,A). Fat cc>lls acciimii- ( Camcwn and Smith, 1964 ) statlies ha~estrongly iir- Icit(d and fill(d fctal poi ciiw ~iilic~itm~~ousddiposc dicatcd iiii cwdotl~c~lialorigin for brown adipocytcs of tissiie in ii vcwtral to tlor sal f,ishion ( Figure 14). Like- tlw rat and IIIOIISC. Thiis, all adipose cells may have wiscb. thc vascular dcvelopmeiit proc(wlct1 along a a conimo~iorigin at the cell level, that being the endo- vcntral to dorsal gradient. thelial or rc,ticular-cndothclial cell. Detelapmentcil Correlate,. Certain dcvclopmetital Rclatiwly iindiffercntiated mesenchymal cells ( of coricllates mist lietwrcn fctal porcino adipose tissiic various shapw ) are normally present, either sparsely and postnatal and inature adiposc, tissue. At all fctal scattered or in small groups bctwcvn adipocytes of ages, the thickness of subcutaneous adipose tissue at iiian (Tcdrschi, 19633, cattlc (Bell, 1909), sheep various anatomicd loc'itions sho~dthe same pattoi 11 ( \\'c~~svoort,1967 ), and thc. pig ( Hcrmans, 1973). as that for backfat thicknesses of- mature pigs ( Figitre Large ntimbcrs of developing red and white blood 13).Sincc me obsc~rvcdthis at n stage (45 days) \vIicn cc~llshavc licwi obscned in white and brown adipose lipid deposition had not begun, the diff cwnce in tissw. Early investigators rcported that the inter- thickness can only he due to difterences in numbers of scapular RL4T of the human (Hatai, 1902; Ronnot, preadipocyte5. Recently EnscLr et 01. ( 1977 ) reportcd 1909; Shattock, 1909), cat and pig ( Ronnot, 1909) that middlc siilxutancwis ( hlSQ ) ,idipocytc~s froin cw~t;iincd viiriahlv 1iiun1)c~rsof lymph antl hacmo- thv shorildc~aid inid-l),ick rc~$on \v(w tlic \am(- si/(., lymph l1(jtl
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FIGURE 10. Paraffin (10 u) section of dorsal subcutaneous adipose tissue of a 9-day old pig stained with the periodic acid Schiff reagents. Showing distribution of multilocular fat cells (m) among unilocular fat cells (u), X 320. Also indicated on the micrograph is the connective tissue septa (cs) between adipose lobules. fat, weight of the fetus or newborn is an accurate and fat-frec carc'iss wcight have. somc. physiological reflecticn of lean body mass. Therefore, there seems relationship in the groning pig. This relationship to be a relationship between lean body mass (body may exist already during fctal growth in the pig. wt. ) and numbers of suhcutaneous prcadipocytes or Enwr et (11. ( 1977') rcyx)rtcd that the hlSQ of thc adipocytr5 ( thickness of backfat) during fetal growth. mid-back ai ('A matiircd c.ar1ic.r than that of the Allen et d.( 1976 j suggc*sted that atlipocyte number shoulc1c.r area in tcwns of cc~swtionof apparcnt adi-
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FIGURE 12. A poroffin section (10 u) of the inner layer of dorsal sub- cutaneous adipose tissue from o three-doy old pig stained with the Hematoxylin Eosin Azure-II stain. A large field showing high numbers of developing blood cells. Severol large clusters of primitive blood cells ore pointed out with arrows, X 135. lndlcated on the rnicrogroph is the muscle- subcutoneous interfoce (m 1 ). pocyte hyperplasia. \Vc have observed that the stroma ing and mclturc pig. The MSQ is the larpst backfat of thc hISQ over the back &eIops earlier than that layer in the mature pig and is the first to de\dop in over the shoulders in fetal deyclopment. Therefore, the fetus ( Figurr 14). We have observed different the direction of developmental gradients present in patterns for layer development in the fetus ( Figurc fcd development may be the same for maturation 14) just as Anderson and Kaiiffman (1973) have gradients in growing pigs. mc>asiircd difirrent growth rates for cach subciitane- oiii layer during postnatal growth. Thus, siibciitanc- Somr relationship5 are l~c~twc~c~i~siibciitanc~oiis 1,iyer o115 adip(iw ti55iw of thc pig does iwt de\~lopor clcvelopment in the fetus and the lxickfat of the grow- grow as a liornogcneous unit, but as tlrrc~wparatr
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viitities (layers) closely associated to each other anatomically.
\’A RI AT10 Ii S it’ithin thr* oritc~layer of p:g subcutancous adipose tissue, we have, observed lobules of adipocytes that arc locatcd around hair follicles (Figure 15). ,41- though they are present in the outcr layer, thc onset of stromal-vascular dcvelopmcnt ( Figure 15) and lipid dcposition (Figure 14) was quite difkrcnt fiom the, rcst of the outer layer. Theye “hair follicle lobules” tailcd to follow the ventral to dorsal gradient for lipid tkposition ( Figure 11) and stromal-vascular develop- mcwt that was prcwnt for the rest of the outer and inner laycr. They arc the largest adipose lobules prcwnt in pig su1)cutaneous and arc probably quiv-
Recrntly, Moody et a!. (1978) compared the hi5to- logical tlcvelopmcmt of subcutancous adipose, tissue lwtwcwi Large LI-hite and Pietrain pigs between birth and 28 days of age. The outer subcutancous 1ayc.r from the Large LI’hite piglc tc \vas more m‘iture ‘it birth and was filled with fat cc,ll~faster thm that of the Pichtrain piglets. Moody and coworkers ( 1978 ) suggested that the tendency for the Pietrain to deposit less carcass fat than Large \Yhite pigs whcn com- pared at 50 kg or more, may already be present at a RE FEliE CES very early age. K Allen, C. E., Thompson, E. H., antl Hegarty, P. V. J. Recently dt PSU we (Hausman, 1978) have mni- 1974. Physiological maturity of muscle and adipose cplls in meat animals. Pmc. Ikciprocal Meat Conf. pared the cellular charactcristics of MSQ 1ic.twcwi 27 :8. O~scili~iw(o1)cw.) and Yorkshirc~ (lean ) pig\
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FIGURE 15
Stromal developw,ent of the adipose lobules around hair follicles, X 125. Paraffin sec- tions (SUI of the outer layer of dorsal sub- cutaneous tissue stained for collagen (Lil- lie’s Allochrome.) A, C, E and G are from lean strain fetuses while B, D, and F are from 105-day fetuses. Note that areas around hair follicles at 60 days (A) are rolid in tissce texture and progressive loos- ening of texture occurs with lobule develop- ment. Also note the earlier onset of this stromal change in the fat strain (8) versuj the lean strain (C) and the larger lobules in the fat strain at later stoges (D, F) versLis the lean strain (E, G). Indicated on the micrographs are hair follicles (hf), epidermis (z), and dc-rmis (d).
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JVisxnsch. (Berlin) 23 :753. Hood, R. I,. 1977. Cellularity of adiposn tissue tlui.inq Bonnot. E. 1908. The inteiwxpulai, gland. .J. Ar?at. Phy- nostnatal develonnient. Proc. Nuti,. Soc. Aust. 2 :43. siol. 43 :43. Iniaeda, T. 1959. The fine structure of human subcutane- Ei,emcr, J. 1937. The protoplasmic filnis of the fat cell. ous fat cells. Arch. hist. .jab. 18:57. the wallL. of the pulmonary alveolus anti the i,enal Jenlcinso;i, D. M., Noble, R. C. and Thompson. G. E. 1968. gloniet.ulus. Anat. Recoid 70 :26::. Adipose tissue and heat production- in the newborn Caniei,on, I. L. and Smith, R. 19+l. Cytological ~IJ- ox (bos taui,us). J. Physiol. 195:639. sponsrs of brown fat tissue E:. in c,)ld exposed rats. .J. Lowe. L. 1978. Zur Kenntniss des Bendegewebes. Archiv. Cell Biol. 23 :89. F. Anat. u. Physiol., Anat. Abth., p. 44. Ching, C. 1940. Some obsewations on the yix?adipo.s:> McCullough, A. W. 1944. Evidence of macrophagal origin cells. Anat. Rec. 77::i97. of zidimse cells in white rat as evidencod by studies Ijrsnoyers, F. and Vodovat~,N. 1974. Api)arition, oi,igine on starved animals. J. Morphol. 75 :193. et evcilution des tissus adipeus c>pitliclvniaii,e et pei,i- Merswann, €1. J., Goodman, J. F. and Brown, L. J. 1975. cardiaque du foetus de porc. Ann. Biol. Anim. Kio- 1)evelopment of swine adiuos- tissue : morphology chin. Riophys. 14:769. and chemical composition. .T. Tipid Res. 16 :269. I)ogliol.ti, G. C. 1928. Ernei.imenta1 stuilirs oii the natu1.e Moody, W. G., Et,s;.!., M. B., Wmd, J. D., Restall, D. J. of adipo5.e tissue using vital staining with arid stains. and Listel,, D. 1978. Comparison of fat and muscle Zychr. Zellforsch. 8:222. development in pietrain and large white piglets. J. Ehrmann, S. 1883. On the formaticn of adipose tis;ue Anim. Sci. 46 :618. from the fatty organs trrined hibcrnatiny gland. Xapolitsno, L. 1963. The differentiation of white adipose Sitzungsb. d. k. Akad. d. Wiisench. (Wien). Math. cells: an electron microscoy)e study. J. Cell Biol. 18: Naturw. Classe. 87:88. 663. Enset., 11. E., Wood, d. I)., Iic!stall, D. .J. antl MacFie, H. Napolitano. T,. antl Fawcett, D. W. 1958. The fine struc- J. €I. 1976. The cellularity of adit-ose tissue from ture of txown adipose tissue in the newhorn mouse pias of diffewnt weights. J. Aqr. Sci. Canib. 86 :633. antl rat. J. Biophys. Biocheni. Cytol. 4:685. Flemniing, JF'. 1871. On the folmstion and i,egi,ession of Poljakoff, P. 1888. A new type of fat forming organ in fat cells in connective tissue with comment on the loose connezti-w tissue. Arch. Mikrosck. Anat. 32 : 123. structure of the lattei,. Ai,ch. 3. niilcr. Anat. 7:32. Ranvier. L. A. 1875. Ti,aite technique d'aistologie. Paris, (;age, S. H. 1882. Oliservations uti the fat cells and con- p. 414. nective tissue eorp s of Nectul.us. Proc. Amer. Shattock, S. G. 1939. On hormonal tumour-like forma- Soc. Microscopists ( tions of fat in man and lower animals. Proc. Roy. (;c~mmel, It. T., Bell, A. ind Alexandei,, G. 1970. Mol,- Soc. Mecl. 2:207. pholoyy of adipose cells in lambs at birth ant1 durin;; Shc!tlon, 13. 1969. The moiyhology and qrowth 3f adi- subsequent transition of I;t.o\vil to white atliimse tis- pose tissue. Proczedings of the Meat Industry Re- sue in warm conditions. Ani. .T. Ant. 133:143. search Conference. American Meat Institute Foun- (;UIT, M. I., Kii,tlantl, J., Phillip, M. and Robinson, M. P. dation, Washington, D. C., pp. 9-23. 1977. The consequenc arly oveimutrition for fat Simon, G. 1965. Histogenesis. I>r : Handbook of Physiol- cell size and nunibe pig as an experimental oqy. Section 5: Adipose Tissue. A. E. Renold and G. model for human ol Inteimational Journal of' F. Cahill,. Ji.., eds. Aniericxn Physiological Society, Obesity 1:151. Washingto.1, D.C., pp. 101-107. Hatai, S. 1902. On thch pi in human embryos of an Tetleschi, C. G. 1965. Patholunical anatomy of adinose interscapular gland ponding to the so-calle(j tissue. It/ :Handbook of Physiology. Section 5: Atii- hibetmating gland of lowc.1. 3ni:nuls. Anat. 4nz. 21 : nose Tissue. A. E. Renold and G. F. Cahill, Jr., eds. :3c;9. American Physio1o:;ical Society, Washington, D.C., II>Iuhman, G. J. 1977. Ce1lu;ar antl histolopical asr:ects of pp. 141-168. developing poi,cine atliimse tissue. Ph.1). Thesis, Uni- Toldt, C. 1870. Conti,ibution to the histology and physi- versity of N'isconsin, Madison. ology of edipose tissue. Sitzber. Akad. Wiss. Wien. Hausman, G. J. and ,Kauffman, I!. G. 1978. The his- Math. Naturwiss. K1. 62:445. tology of developing porcine atlipose tissue. Sub- Waldeyer, 1875. About coanective tissue cells. Arch. mitted to Journal of Lipid Research. Mikroskop.W. Anat. 11 :176. EIzusman, G. J. 1978. Unpublished obse1,vations. IIchi.nians, P. G. C. 1973. The development of adipose tis- Warthin, A. S. 1903. On the development of hemolymph (j: SLIC iil swine foetuses (a morphological stutly). noties in adipose tizsue. Proc. Pathol. SOC. Phila. Ti j (1 sc h r . D i ei,: