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81974929.Pdf View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Keratinocytes Play a Role in Regulating Distribution Patterns of Recipient Melanosomes In Vitro Ljiljana Minwalla, Yang Zhao, I. Caroline Le Poole,* R. Randall Wickett,² and Raymond E. Boissy Department of Dermatology and ²Department of Pharmaceutical Sciences, University of Cincinnati, Cincinnati, Ohio; *Department of Pathology, Loyola University of Chicago, Maywood, Illinois, U.S.A. Melanosomes in keratinocytes of Black skin are lar- versus clustered in (i) 77% vs 23% and (ii) 64% vs 36%, ger and distributed individually whereas those within respectively. In contrast, when keratinocytes from keratinocytes of Caucasian skin are smaller and dis- light skin were cocultured with melanocytes from (iii) tributed in clusters. This disparity contributes to dif- dark skin or (iv) light skin, recipient melanosomes ferences in skin pigmentation and photoprotection, were individual versus clustered in (iii) 34% vs 66% but the control of these innate distribution patterns and (iv) 39% vs 61%, respectively. These results indi- is poorly understood. To investigate this process, cate that recipient melanosomes, regardless of origin, cocultures were established using melanocytes and are predominantly distributed individually by kerati- keratinocytes derived from different racial back- nocytes from dark skin, and in membrane-bound grounds and were examined by electron microscopy. clusters by those from light skin. There were also Melanosomes transferred to keratinocytes were cate- differences in melanosome size from dark or light gorized as individual or in various clusters. donor melanocytes. Melanosome size was not related Melanosome size was also determined for individual to whether the melanosomes were distributed indi- and clustered melanosomes. Results indicate that, in vidually or clustered, however, in cocultures. These our model system, melanosomes in keratinocytes results suggest that regulatory factor(s) within the from different racial backgrounds show a combin- keratinocyte determine recipient melanosome distri- ation of clustered and individual melanosomes. bution patterns. Key words: cocultures/melanocyte/ When keratinocytes from dark skin were cocultured pigmentation/skin color. J Invest Dermatol 117:341±347, with melanocytes from (i) dark skin or (ii) light skin, 2001 however, recipient melanosomes were individual elanosomes transferred within keratinocytes of speci®c mechanisms have been proposed for melanin-mediated dark skin individuals are predominantly distrib- photoprotection. They include the ®ltering and attenuation of uted as individual organelles throughout the impinging radiation by scattering, absorption, and subsequent cytoplasm, with an increased density apically over dissipation (as heat), absorption accompanied by redox reactions, Mthe nucleus, of both sun-exposed and nonex- and absorption accompanied by electron transfer processes (Kollias posed skin. In contrast, three to eight melanosomes clustered into et al, 1991). membrane-bound groups predominate within keratinocytes of Regardless of mechanisms by which melanin attenuates the Caucasians (Szabo, 1969; Konrad and Wolff, 1973; Jimbow and effects of UV radiation, the melanosomes shield the keratinocytes' Sugiyama, 1998). These clusters also accumulate in the supranuclear nuclear DNA from these damaging rays by forming a protective position in light skin keratinocytes. The distribution patterns of ``cap'' over the nuclei. It was postulated that clustered melanosomes melanosomes within keratinocytes are one determining factor in in Caucasian keratinocytes redistribute into single entities within skin color. The distribution of single melanosomes increases light the keratinocytes upon UV exposure to more ef®ciently shield the absorption exhibited physiologically by a darker skin color. More nuclei (Toda et al, 1972; Jimbow et al, 1991). Thus, the constitutive importantly, this distribution plays an important role in photo- and facultative distribution of melanosomes within keratinocytes is protection. In fact, it is widely agreed that melanin and the of primary concern with regard to the damaging effects of radiation, distribution of melanosomes in the epidermis are the most and this differs widely between different skin colors. The mech- important factors in the protection of human skin from the anism regulating the constitutive distribution of melanosomes detrimental effects of ultraviolet (UV) light. Much of this within keratinocytes has not been elucidated, however. protection is offered by the fact that melanin can absorb effectively Whereas the mechanism of melanosome transfer from melano- throughout the visible and UV electromagnetic spectrum. Various cytes to keratinocytes is not fully understood, some studies indicate that the mode of transfer of melanosomes, either singly or as Manuscript received October 19, 2000; revised February 19, 2001; clusters, is a melanocytic-dependent process and is responsible for accepted for publication March 15, 2001. constitutive differences in distribution patterns of melanosomes. Reprint requests to: Dr. Raymond E. Boissy, Department of Recently, Bessou-Touya et al (1998) established heterologous Dermatology, University of Cincinnati, PO Box 670592, Cincinnati, melanocyte±keratinocyte reconstructions and examined them Ohio 45267-0592. Email: [email protected] macroscopically and microscopically. Their conclusions suggested 0022-202X/01/$15.00 ´ Copyright # 2001 by The Society for Investigative Dermatology, Inc. 341 342 MINWALLA ET AL THE JOURNAL OF INVESTIGATIVE DERMATOLOGY that epidermal pigmentation is determined by the melanocyte All cultures were maintained in a tissue culture incubator at 37°C phototype. with 5% CO2. Growth medium was routinely changed twice a week. Other studies indicate a correlation between melanosome size Electron microscopy For ultrastructure of the skin, a 3 mm diameter and the distribution pattern of melanosomes within secondary punch biopsy was obtained from the forearm of an African American lysosomes of keratinocytes. Melanosomes larger than 1 mm are and a Caucasian adult with informed consent and ®xed with half- singly distributed, whereas those smaller than 1 mm in long axis are strength Karnovsky's ®xative overnight at 4°C as previously described aggregated to form melanosome complexes (Szabo, 1969; Toda et (Boissy et al, 1991). The tissue was then cut into quarters and processed al, 1972; Wolff et al, 1974; Yamamoto and Bhawan, 1994; Jimbow for routine electron microscopy as described below. and Sugiyama, 1998). These observations have led investigators to For the ultrastructural study of cultured cells, primary melanocytes were cocultured for 4 d with primary keratinocytes at a ratio of 1:2, suggest that a melanosome-associated signal regulates its distribu- respectively, and maintained in 1:2 normal melanocyte growth medium tion pattern in the recipient keratinocyte (Wolff and Konrad, 1971; to normal keratinocyte growth medium, respectively. Cells were seeded Jimbow and Sugiyama, 1998). This hypothesis was tested and into one-well Laboratory-Tek chamber slides (Nunc, Naperville, IL). On supported experimentally by observing phagocytosis by keratino- the ®fth day, adherent cells were processed for electron microscopy as cytes of either isolated melanosomes or latex beads of different previously described (Boissy et al, 1991). Brie¯y, cells were ®xed in wells particle sizes (Korn and Weisman, 1967; Wolff and Konrad, 1971; with half-strength Karnovsky's ®xative in 0.2 M sodium cacodylate buffer 1972). at pH 7.2 for 30 min at room temperature. When using melanocytes In contrast, there have been reports demonstrating that derived from light skin, it was necessary to stain the melanosomes for melanosome size does not correlate with their distribution pattern improved visualization by incubation in l-dihydroxyphenylalanine (DOPA), which reacts with tyrosinase to yield a brown/black polymer- within keratinocytes. In some pigmentary disorders and after ous end product, both in situ and post®xation. For in situ DOPA certain chemical treatments, the melanosome distribution in treatment, 250 mM L-DOPA was added to the medium on days 1 and 2 secondary lysosomes is not consistent with their size (Jimbow and for 5 h each day. For post®xation DOPA histochemistry, ®xed cells were Sugiyama, 1998). In Caucasians, for example, nitrogen mustard incubated in a 0.1% solution of L-DOPA twice for 2.5 h (Boissy et al, treatment of skin produces a condition in which almost all of the 1991). All cells were then washed three times in buffer and treated with small melanosomes are singly distributed rather than forming 1% osmium tetroxide containing 1.5% potassium ferrocyanide for melanosome complexes in keratinocytes as expected (Flaxman et al, 30 min. The cells were washed, stained en bloc with 0.5% uranyl acetate 1973). Because melanosome size has not been altered, some other for 30 min, dehydrated, and embedded in Eponate 12. For one sample controlling property might have changed. Furthermore, Bhawan et of each type of coculture, 10 areas of each coculture were cut out of the Epon cast, mounted on Epon pegs, and sectioned on an RMC MT al (1976) conducted an ultrastructural study of pigmentary abnor- 6000-XL ultramicrotome. Ultrathin sections were then stained with malities including melanosome size, shape, and distribution in aqueous solutions of uranyl acetate (2%) and lead
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