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Cellular and Histological Aspects of Developing Porcine Adipose Tissue

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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 - 35 - AMERICAN MEAT SCIENCE ASSOCIATIGN 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). -36- AMERICAN MEAT SCIENCE ASSOCIATION 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$, 1973) and lire 6). Presumptive adipow lobules are the source of ovine ( Wensvoort, 1967) adipore tis5ue. We ha\e adipocytcs and capillaries of developing fat cell dcxxibed the formation of presumptive adipose lob- clustcm (Figure 7). The cells of the presumptive ules in porcine adiposc tissiic (Figure 6). The pre- lobules either lwcomc adipocytes or the endothelial sumptivc lobules were formed by the condensation cells of thc. capillary walh. - 37 AMERICAN MEAT SCIENCE ASSOCIATION Sinal1 unilocular cells and multilocnlar cells havc PRESUMPTIVE ADIPOSE TISSUE I)cwi observed continiiously in postnatal pig adipotcb (hlc.rsmann et n7, 1975), up to and including 150 days of age. ORGAN TION The literaturc contains much c~idcncrfor an cndo- thelia1 or reticular-endothelial origin for hrown and BAT, rat, rabbit, cat white adipocytes. \hny studics have indicated a close dcwclopmental relation5hip betwclen adipocytes and ORGANIZATION CELLULAR LIPID blood vessels ( Flcmming, 1871, Toldt, 187’0; Rmvicr, RESULTING IN / DEPOSITION BEGINS A COMPLETE 1875; Pollakoff, 1888, \l’assc.rinann, 1965, Barnard, CONNECTIVE 1F69; Kapolitano, 1963; Sheldon, 1969; Naplitano aid TISSUE BORDER BAT, sheep Fawcett, 1955, Simon, 1965; Imaeda, 1959; I)esiioyc.rs AROUND A GROUP OR GROUPS OF and Vodovar, 1974; Bell, 1909 ). Adipogenesis was ADIPOCYTES WAT, cattle bound to proliferation of blood vessclls in subcutanc- LIS tissue (Simon. 1965, Flcmming, 1871 ), and iii thc F WAT, pig, human mouse epididymal fat pad (Wassermann, 1965). In sheep ( \Vc.nsvoort, 19671, pig ( Hermans, 1973), hu- man and rat (Simon, 1965) adipose tissue, perivas- MATUl ION cular reticulum cells were considcred “~~r~~adipocytcs.” \Vasscnnann’$ ( 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.
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