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Invited Review the Phylogenetic Odyssey of the Erythrocyte. IV. The

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Invited Review the Phylogenetic Odyssey of the Erythrocyte. IV. The Histol Histopathol (1997) 12: 147-170 Histology and 001: 10.14670/HH-12.147 Histopathology http://www.hh.um.es From Cell Biology to Tissue Engineering Invited Review The phylogenetic odyssey of the erythrocyte. IV. The amphibians C.A. Glomski, J. Tamburlin, R. Hard and M. Chainani State University of New York at Buffalo, Department of Anatomy and Cell Biology, School of Medicine, Buffalo, New York, USA Summary. Amphibians mani fes t permanently nucleated , Introduction oval. flatte ned , biconvex ery throcytes. These cell s demonstrate a cytoskeleton which is responsible for their H e moglo bin is a n unique, a nc ie nt respirato ry morphogeneti c conversion from a sphere to an ellipse me ta ll o -pig m e nt w hose s pec ia li zed func ti o ns a nd imparts to the ir cellular m ass revers ibility of a re d e mo ns tra bly e nha nced by it s m ic ro ­ traumati c deformati o n. The class Amphibia has the environmentali zati on in a passive-flowi ng, circulating largest of all erythrocytes attaining volumes greater than cell as opposed to free physical solution in the plasma as 10,000 fe mto lite rs in the Amphiuma. The la rge seen at the in vertebrate level (Glomski and Tamburlin, dimensions re fl ect evolutionary processes, genomic size, 1989). The degree of its polymeri zati on, association with plo id y a nd the re lative size of o the r somati c cell s. interactive enzyme syste ms, and the structure o f it s Conversely, the ery throcyte count a nd he mog lobin globin chains confe r upon the compound a spectrum of concentrat io n of these spec ies are low. Occasio na l qualities of oxygen binding/release that can be viewed as denucleated red cell s can be seen in the peri pheral blood tail ored for cert ain stages of life (e.g. embryonic vs. but may attain levels of 90-95% of the total circ ulating adult) and specifi c organis ms . The e mergence of the populati on in certain members of the tribe Bolitoglossini earli est erythrocytes in certain in vertebrates and the (e.g. Batrachoseps attenuatus). These erythropl astids phenomenon of eryth ropoiesis in the lowest vertebrates, reta in the ma rg in a l ba nd thu s re ma ining diffe re nt the primitive (cartilagino us) and modern (bo ny) fish fro m ma mma li a n eryth rocy tes. E mbryo log icall y, have been appraised in subsequent reports of this series e ry thro po iesis initia tes in the yo lk sac a nd the n (Glomski and Tamburlin , 1990; Glomski et a I. , 1992). progresses to the kidney, li ver, and possibly spleen. The The pi sc ine e ry throcy te a lo ng with its m o d e of yolk sac cohort is transitory and is successively replaced producti on can be considered prototypes of this cell and by the larva l and definitive populati ons of erythrocytes. it s ge nes is thro ug ho ut a ll o the r s ubmamma lian Red cell production (along with th rombocytopoiesis) in vertebrates. The establishment of transient and definitive ad ult urodeles is conducted intravascularl y in the spleen. populati ons of erythrocytes, generati on of red cells in a In anurans this organ is usuall y the major site although ce rta in g ro up of o rgans, a nd the e la bo ra ti o n o f the li ver a lso serves as a seconda ry locus fo r this erythrocytes with reasonabl y characteri stic dimensions, ac ti vity. Medullary (bone marrow) erythropoiesis makes hemoglobin concentrations, and other cytologic features its ph y loge ne t ic d e but in a nura ns a nd ty picall y in coho rts s uc h as fa mil ies a nd s pec ies o f the occ urs d ur in g he ig hte ne d he m o po ies is foll ow in g chondroichthyes and osteichthyes is paralleled at higher me ta morphos is o r hibe rn a ti o n . M a turati o n of the phylogenetic levels . Many fac tors that have an impact e ry th rocy te in the c irc ul a ti o n is commo nplace upon erythrocellular qua lities and values have been (especiall y in urodeles) while proli fe rati on at this site is ide ntified . The purpose of the present re port is to in d uc ibl e by s pl e nec to m y a nd/or he m o lys ins. consider erythropoiesis at the next phylogenetic level, Ery throcy te -re la te d va lues d e m o ns trate vari a ble i .e. among the me mbe rs o f the c lass Amphibia. di ffe rences associated with age, weight , season, gender, Erythropoieti c development in amphibians readily lends and environment. itself to the experimental identification and delineati on of the precepts that this process observes. Furthermore, it Key words: Erythrocyte, Eryth ropoiesis, Hemopoiesis, offers an insight into and is somewhat predicti ve of this Hemoglobin , Amphibian, Bone marrow acti vity in higher animals including man. The A mph ibia ns we re the f irs t ve rte brates to Offprint requests to: Professor Chester A. Glomski, State University of a ba ndo n evolutio na ril y a n exc lu s ive ly aquat ic New York at Buffalo. Department of Anatomy and Cell Biology, School envi ro nment and adopt respirato ry mechani s ms that of Medici ne, Sh erman Hall 309, Buffalo, New York 14214, USA permit a terrestro-aquatic existence. Consequently larval 148 Erythrocyte odyssey gills are likely to be replaced by lungs in adults and Some salamanders replace their lost gills with lungs cutaneus respiration is also adopted. Indeed, in some while others (Plethodontidae) do not. Both types of cases lungs are acquired even though gills are urodeles nevertheless, along with the (lunged) anurans, permanently retained. Amphibians' erythrocytes express utilize cutaneous respiration which is accomplished by the cytologic characteristics that these cells present in extensive capillary beds within the epidermis. Among fish. However, they also manifest changes presumably newts 75% of respiratory exchange is cutaneous while reflective of their hosts' new habitat and activities. Their the lungs supply the rest. In lungless salamanders the structural dimensions, number in circulation and other skin is responsible for an even greater proportion with aspects of cellular expression are particularly varied , the remainder being effected by the buccal mucous often novel. As in fish , the earliest erythropoietic activity membranes. Cutaneous respiration accounts for occurs in the yolk sac followed by internal organs as the approximately 30% of the oxygen absorption in the kidney, spleen , or liver. Some amphibians further aquatic African clawed toad Xenopus laevis and 50% in incorporate a new erythropoietic locus, the bone marrow, Rana esculenta , the edible frog (Foxon , 1964). which has been subsequently universally adopted by the Cutaneous oxygen consumption in the Andean frog higher vertebrates. Telmatobius marmoratus exceeds its pulmonary uptake by 40-60% (Ruiz et aI. , 1983). Awareness of this method Taxonomic organization of oxygenation aids in understanding how some amphibian can repeatedly switch from gaseous to The amphibians are so-named because most aquatic environments (or vice versa) without difficulty, members lay their eggs in water which develop into as well as how hibernation under various conditions aquatic larvae and subsequently undergo metamorphosis becomes tolerable. The efficacy of cutaneous respiration into terrestrial adults. Thus, they live in both aquatic and is implied by the observation that some anurans and terrestrial environments. All surviving amphibian urodeles completely devoid of erythrocytes and plasma species are included in three orders, the Caecilia, hemoglobin can still maintain their existence (DeGraaf, Urodela (Caudata or tailed amphibians) and Anura 1957; Ewer, 1959; Grasso and Sheppard, J968). (tailless amphibians). The simplest are the caecilians The erythrocytes of an amphibian were first which are wormlike animals without limbs, limbgirdles observed by Leeuwenhoek (1683 , 1722) when he or a significant tail. Their body is segmented by circular examined the blood of a frog with his microscope. He folds, the skin is smooth and devoid of scales. Caecilians noted and illustrated their oval configuration (Fig. I). are tropical, fossorial creatures that burrow and live in The credit of recognizing the shape of the red blood cells forest soil and river banks. The sirens (members of the throughout the Amphibia, their inordinately huge Urodela) conversely, though elongated and somewhat dimensions in some urodeles and their otherwise large wormlike, have a pectoral girdle with tiny front legs but size in the rest of this class, however, belongs to George no hind limbs. They have external gills and a distinct Gulliver. Thi investigator, the author of hematology'S tail. Sirens are exclusively aquatic , have a limited counterpart of «Gulliver ' s Travels.» (i.e. his distribution in the USA, and only a few species are «explorations» in comparative erythrology), described extant. Salamanders have both fore- and hindlegs, a and compared erythrocytes throughout the classes and distinct neck between the head and long body, and a orders of vertebrates. His 1862 and 1875 reports permanent tail. Salamander larvae in all but rare presented woodcuts than dynamically document the instances are aquatic , developing in permanent or morphology of the amphibians' erythrocytes in context temporary, and even subterranean waters.
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