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Aging of Melanocytes

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Aging of Melanocytes oo22-202X/79/730 1-0070$02.00/0 THE .JOURNAL OF I NVESTI GATIVE DERMATOLOGY, 73:70-79, 1979 Vo l. 73, No.1 CopyrighL © 1979 by T he Williams & Wilkins Co. Pril/.ted il/. U. S. A. Aging of Melanocytes FUNAN Hu, M.D. DiVl:sion of Cutaneous Biology, Oregon Regional Primate Research Center, Beaverton, Oregon, U.S.A. Choroidal m elanocytes of the eyes of postnatal animals sufficient numbers. Only then do they cease division, become are classified as postmitotic terminally differ entiated organized as specia lized tissue, a nd serve their specific func­ cells. They have specific granules, the melanosomes, tions. Apparently the orga nism does not requil-e periodic re­ which unde rgo changes qualitatively and quantitatively plenishment of these celJ s, which, once formed, are expected to correlated to the animal's increasing age. Epidermal last for the life of the organism. melanocytes, which normally divide only on demand or We have demonstrated t hat choroidal melanocytes of adult by stimulation, are classified as intermittent mitotic eyes are postmitotic, terminalJy differentiated cells [7]. Ob­ cells. During their development, le ntigines and nevi of viously, we could not use the cell's inability to divide as the the skin show progressive ultrastructural and cytochem­ indicator of aging cha nges. Because melanocytes synthesize a ical changes s imilar to those in the choroidal ce lls, and specific enzyme a nd produce a characteristic product, the m el­ thus may be considered a s aging populations of skin anosomes, we logically assumed that a decline in these well­ melanocytes. These facts have led to the conclusion that recognized functions was associated with aging. choroida l melanocytes may be used advantageously as a model for studying changes in cells from maturation MATERIALS AND METHODS to senescence. Eyei; of Rhei;us Macaques Eyes from rh esus (Macaca mulatta) fetuses of gestational ages Diploid human fibroblasts in culture change from rapidly va rying from 65 days to 165 days (term) and eyes from newborn, infant, replicating (phase I), to slowly rephcating (phase II) , to nonrep­ adolescent, yo un g ad ults, and old adults of different ages were used. All licating (phase III) cells [1]. Their life span, in terms of the eyes were removed aseptically, soaked in several changes of Hanks' number of population doublings, depends upon the age of the balanced salt solu tion with antibiotics, and cut anteroposleriorly into 4 parts. After the removal of the crystalline lens and the vitreous, the donor [2,3]. Fibroblasts from young individua ls proliferate more pigmented membrane (the iris, ciliary body, and choroid with their times than those from old people, but the sum total of theil' corresponding pigment epithelium ) was exposed. population doubling is a constant characteristic of the species. For histological study, a strip of the pigmented membrane was fix ed Although investigators have proposed several hypotheses to in 10% buffered neutral formalin and prepared for paraffin section ing. explain this observation [4,5], so far no one has adequately Another strip was frozen and sectioned for enzyme studies. explained th e m echanisms of aging operating in all cells. Most For electron microsco py, strips were fixed in 2.7% glutaraldehyde in investigators have emphasized changes in the ability of cells to Millonig's phosphate buffer [8] at pH 7.4 for 1 hr. While in the fi xative, divide as indicators of t he aging process. However, not all the tissue was divided in to iris, ciliary body, and choroid-retina and cut postnatal mammalian cells divide continuously; some replicate in to pieces (about 1 mm"). One-half of these pieces were incubated in 0.1% 1,-3,4-dihydroxyphenylalanine (dopa, Sigma Chemical Co mpany) only intermittently, and some stop dividing early in postnatal in phosphate buffer at pH 7.4 for 5 hl' and postfixed for 90 min ill cold life. 1% OsO" in cacodylate buffer [9]. Control pieces were in cubated in the Basal epithelial cells of the epidermis divide continuously buffer without dopa and were processed in an identical manner. The because they differentiate into a dead product, keratin. When pieces were then washed, dehydJ'ated in a series of graded alco hol epidermis is grown in cult ure, the mitotic rate generally is not solu tions, and embedded in Spurr [10]. One-micrometer sections were in keeping with the rate of keratinization, and the culture dies. cul and stained with to luidine blue so that specific areas or ce lls co uld Given an optimal environment, however, these cells can prolif­ be selected for ultrathin sectioning with a Porter-Blum MT-2 ultl'ami- I erate continuously [6]. crotome. Ultrathin sections were stain ed with uranyl acetate and lead Fibroblasts and epidermal melanocytes in vivo are intermit­ citrate [11], and examin ed with a Philips 200 electron microscope. tently mjtotic, but both fibroblasts and m ela nocytes, in certain Human Skin stages of their lives (for instance, during embryonic develop­ ment), must be rapidly replicating if the organism is to acquiTe Biopsy samples were taken from lesions diagnosed clinically as lentigo simplex; lentigo senilis; mu ltiple lentigines syndrome; nevus t he population of these cells it requires. At certain stages of spilus; junctional, compound, and in traderm al nev us; lentigo maligna; development the rate of proliferation changes; the cells become and superficial malignant melanoma. Each sampl e was cut in lo halves. differentiated and acquire the specific properties that charac­ One was processed routinely and stained with hematoxylin-eosin; the terize the particulru' cell types. Only at this time do these celJ s other was processed for electron microscopy. Like the rhesus eye become intermittently mitotic. After this ' stage has been tissues, the latter specimens were again divided in to 2 parts. One part reached, they are required to replicate only when cell injury or was in cubated in dopa reagent and the other was used as a control. death occurs or when extra demands a)'e placed upon their Otherwise both were processed in an identical fashion. numbers or products. Muscle and nerve cells are non mitotic. These cells also must RESULTS go t ru'ough the continuously mitotic stage until they reach Choroidal M elanocytes Melanocytes of aU ages were fIlled with brown or brownish T he work described in this article, Publication No. 1020 of the black m elanin pigment granules (melanosomes) that appeared Oregon Regional Primate Research Center, was supported in part by dark green in toluidine-blue- or Giemsa-stained sections. In the Publi c Health Service, National Institules of Health grants ORR 00163 of' the Animal Reso urces Branch, Division of Research Resources, AM young a nimals, e.g., newborns to 3-yr-olds, these granules were 0844 5 of the National Institute 0 (' Arthritis, Metabolism and Digestive uniform in color, size, and shape (Fig 1) . Melanosomes at age 7 Diseases, and EY 02086, Retinal and Choroidal Diseases, National Eye under a li ght microscope were still -uniform. But under an Inslitute. electron microscope we observed that a few of these granules Reprin t req uests to: Funan Hu, M.D. , Division of Cutaneo us Biology, had lost some electron density. Adults (12 to 13 yr of age) had Oregon Regional Primate Research Center, Beaverton Oregon 97005. considerable numbers of melanosomes that val'ied in size and 70 July 1979 AGING OF MELANOCYTES 71 FIG 2. Choroidal melanocytes from a rhesus macaque over 12 yr of FIG 1. Choroid al melanocytes from the eye of a 3-yr -o ld rhesus age. The melanosomes show vacuolization and form melanosome com­ macaque. T he melanosomes appeal' unifo rm in size and electron den­ pl exes. Bar = 1 /lm . Inset: a higher-magnification photograph showing oity. Bar = 1 /lm. Inset: a higher-magnification photograph showing melanosome details. melanosome details. in color and that appeared vacuolated (Fig 2). In toluidine-blue­ stained sections, the granules did not stain uniformly dark green, but rather varied from dark green, to ljght green, to brown, to light brown. In the eyes of animals at least 15 yr of age, more than 60% of the melanocytes showed extensive alterations in the melano­ somes; almost all cells had some altered granules. Under an electron microscope, the changes were more obvious. Melano­ somes showed extensive loss of electron density and resembled vacuoles fllied either completely or partially with a homogene­ ous material of a low density. Some vacuoles had electron-dense cores of varying size and shape, some had dense or lighter cores, and some had cores that were half-dense, half- light. Some melanosomes appeared fused together as a melanosome com­ plex enclosed by a unit membrane (Fig 3). Table 1* shows the percentage of melanocytes that had extensively altered mela­ nosomes. About 10 to 15% of melanocytes had changes at age 7, 50% at age 13, and more than 60% at 15. Indeed, in animals more than 15 yr of age, almost all melanocytes had some altered melanosomes, and more than 60% had extensive changes. Lentigo Simplex, Lentigo Senilis, Mu.ltiple L entigines Syndrome, and Nevus Spilus Lentigo simplex tissue showed a slight elongation of the rete ridges, an increase in the concentration of melanocytes in the basal layer, an increase in the amount of melanin in both the melanocytes and the basal keratinocytes, and melanin-contain­ ing macrophages in the dermis [12]. T hese changes became exaggerated in lentigo senilis, which had elongated and hyper- • The age of the adult animals is an approximation only. Because the adults were not. born 01' raised at the Oregon Regional Primat.e FIG 3.
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