Extradermal melanin transfer? Lack of macroscopic spleen melanization in old C57BL/6 mice with de-synchronized hair cycle

• Authors: Dominika Michalczyk , Malgorzata Popik , Aleksander Salwinski , Przemyslaw M Plonka
• Languages of publication: EN

Abstracts

EN

In quest of alternate, extradermal path of melanin transfer from skin to the visceral organs, we suggested that some portions of such melanin may be deposited in the spleen, which in young black C57BL/6 mice is often melanized. Here, we confirm these observation using young C57BL/6 female mice (up to 17 weeks) and show that this phenomenon cannot be observed in old animals where the hair cycle is not synchronized any more. The experiments were carried out both on spontaneous and depilation-induced hair cycle. We have checked it as a side-observation over many other experiments carried out on young and old C57BL/6 female mice (up to 2.5 years of life). The presence or absence of melanin in the spleens was checked macroscopically, and histologically by Fontana-Masson (FM) staining, and synchronization of the hair cycle - by standard histomorphometric analysis of the back skin hair follicles. In about 40% of old spleens black FM-stainable 'debris' could be found under closer histological examination. This study shows that, at least in part, the phenomenon of splenic melanosis in C57BL/6 mice can be correlated with the synchronized skin melanization parallel to the hair cycle progress, and that splenic melanin undergoes gradual degradation during the mouse life.

Keywords

EN

lipofuscin; Fontana-Masson staining; melanin degradation; spleen melanosis; ageing; hair cycle

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2009
• Volume: 56
• Issue: 2
• Pages: 343-354

Dates

published

2009

received

2009-04-07

revised

2009-06-04

accepted

2009-06-17

(unknown)

2009-06-18

Contributors

author

Dominika Michalczyk

• Department of Biophysics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland

author

Malgorzata Popik

• Department of Biophysics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland

author

Aleksander Salwinski

• Department of Biophysics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland

author

Przemyslaw M Plonka

• Department of Biophysics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland

References

• Bancroft JD, Stevens A (1982) Theory and practice of histological techniques. Churchill Livingstone, Edinburgh, Scotland.
• Borovansky J, Elleder M (2003) Melanosome degradation: fact or fiction. Pigment Cell Res 16: 280-286.
• Bryniarski K, Biedron R, Jakubowski A, Chlopicki S, Marcinkiewicz J (2008) Anti-inflammatory effect of 1-methylnicotinamide in contact hypersensitivity to oxazolone in mice; involvement of prostacyclin. Eur J Pharmacol 578: 332-338.
• Chase HB (1954) Growth of the hair. Physiol Rev 34: 113-126.
• Chase HB, Eaton GJ (1959) The growth of hair follicles in waves. Ann N Y Acad Sci 83: 365-368.
• Crichton DN, Busuttil A, Price WH (1978) Splenic lipofuscinosis in mice. J Pathol 126: 113-120.
• Double KL, Dedov VN, Fedorow H, Kettle E, Halliday GM, Garner B, Brunk UT (2008) The comparative biology of neuromelanin and lipofuscin in the human brain. Cell Mol Life Sci 65: 1669-1682.
• Dry FW (1926) The coat of the mouse (Mus musculus). J Genet 16: 281-340.
• Fontana A (1912) Verfahren zur intensiver und raschen Farbung des Treponema pallidum und anderer Spirochäten. Dermatol Wochenschr 55: 1003-1004 (in German).
• Goyarts E, Muizzuddin N, Maes D, Giacomoni PU (2007) Morphological changes associated with aging: age spots and the microinflammatory model of skin aging. Ann N Y Acad Sci 1119: 32-39.
• Grimelius L (2008) Methods in neuroendocrine histopathology. A methodological overview. Upsala J Med Sci 113: 243-260.
• Hansen LS, Coggle JE, Wells J, Charles MW (1984) The influence of the hair cycle on the thickness of mouse skin. Anat Rec 210: 569-573.
• Hendrix S, Handjiski B, Peters EM, Paus R (2005) A guide to assessing damage response pathways of the hair follicle: lessons from cyclophosphamide-induced alopecia in mice. J Invest Dermatol 125: 42-51.
• Hill HZ, Hill GJ (1987) Eumelanin causes DNA strand breaks and kills cells. Pigment Cell Res 1: 163-170.
• Ishiyama T, Klinkosz B, Pioro EP, Mitsumoto H (1997) Genetic transfer of the wobbler gene to a C57BL/6J × NZB hybrid stock: natural history of the motor neuron disease and response to CNTF and BDNF cotreatment. Exp Neurol 148: 247-255.
• Izumi T, Gomi H, Kasai K, Mizutani S, Torii S (2003) The roles of Rab27 and its effectors in regulated secretory pathways. Cell Struct Funct 28: 465-474.
• Kayatz P, Thumann G, Luther TT, Jordan JF, Bartz-Schmidt KU, Esser PJ, Schraermeyer U (2001) Oxidation causes melanin fluorescence. Invest Ophthalmol Vis Sci 42: 241-246.
• Kent S (1976) Solving the riddle of lipofuscin's origin may uncover clues to the aging process. Geriatrics 31: 128-137.
• Korytowski W, Pilas B, Sarna T, Kalyanaraman B (1987) Photoinduced generation of hydrogen peroxide and hydroxyl radicals in melanin. Photochem Photobiol 45: 185-190.
• Kostanecki W, Kwiatkowska E, Zak R (1967) The effect of Endoxan on hair melanogenesis and hair growth in mice. Arch Klin Exp Dermatol 230: 396-401 (in German).
• Masson P (1914) La grande endocrine de l'intestin chez l'homme. CR Acad Sci (Paris) 138: 59-61 (in French).
• Militzer K (2001) Hair growth pattern in nude mice. Cells Tissues Organs 168: 285-294.
• Milner Y, Sudnik J, Filippi M, Kizoulis M, Kashgarian M, Stenn K (2002) Exogen, shedding phase of the hair growth cycle: Characterization of a mouse model. J Invest Dermatol 119: 639-644.
• Mueller-Roever S, Handjiski B, van der Veen C, Eichmuller S, Foitzik K, McKay IA, Stenn KS, Paus R (2001) A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol 117: 3-15.
• Palumbo A (2003) Melanogenesis in the ink gland of Sepia officinalis. Pigment Cell Res 16: 517-522.
• Paus R, Christoph T, Müller-Röver S (1999) Immunology of the hair follicle: a short journey into terra incognita. J Investig Dermatol Symp Proc 4: 226-234.
• Paus R, Handjiski B, Eichmüller S, Czarnetzki BM (1994) Chemotherapy-induced alopecia in mice. Induction by cyclophosphamide, inhibition by cyclosporine A, and modulation by dexamethasone. Am J Pathol 144: 719-734.
• Paus R, Stenn KS, Link RE (1990) Telogen skin contains an inhibitor of hair growth. Br J Dermatol 122: 777-784.
• Plikus MV, Chuong CM (2008) Complex hair cycle domain patterns and regenerative hair waves in living rodents. J Invest Dermatol 128: 1071-1080.
• Plikus M, Chuong CM (2004) Making waves with hairs. J Invest Dermatol 122: vii-ix.
• Plonka P, Plonka B, Paus R (1995) Biophysical monitoring of melanogenesis as a tool for pigment and hair research. Arch Dermatol Res 287: 687-690.
• Plonka PM, Handjiski B, Popik M, Michalczyk D, Paus R (2005a) Zinc as an ambivalent but potent modulator of murine hair growth in vivo - preliminary observations. Exp Dermatol 14: 844-853.
• Plonka PM, Michalczyk D, Popik M, Handjiski B, Slominski A, Paus R (2005b) Splenic eumelanin differs from hair eumelanin in C57BL/6 mice. Acta Biochim Polon 52: 433-441.
• Plonka PM, Michalczyk D, Popik M, Handjiski B, Paus R (2008) Electron paramagnetic resonance (EPR) spectroscopy for investigating murine telogen skin after a spontaneous or depilation-induced hair growth. J Dermatol Sci 49: 227-240.
• Romeis B (1991) Mikroskopische Technik. Urban & Schwarzenberg, Muenchen, Germany (in German).
• Roméro-Graillet C, Aberdam E, Aberdam E, Biagoli N, Ortonne J-P, Ballotti R (1996) Ultraviolet B radiation acts through the nitric oxide and cGMP signal transduction pathway to stimulate melanogenesis in human melanocytes. J Biol Chem 271: 28052-28056.
• Roméro-Graillet C, Aberdam E, Clément M, Ortonne J-P, Ballotti R (1997) Nitric oxide produced by ultraviolet-irradiated keratinocytes stimulates melanogenesis. J Clin Invest 99: 635-642.
• Rozanowski B, Cuenco J, Davies S, Shamsi FA, Zadlo A, Dayhaw-Barker P, Rozanowska M, Sarna T, Boulton ME (2008) The phototoxicity of aged human retinal melanosomes. Photochem Photobiol 84: 650-657.
• Sarna T, Plonka PM (2005) Biophysical studies of melanin: paramagnetic, ion-exchange and redox properties of melanin pigments and their photoreactivity. In Biomedical ESR. Biological Magnetic Resonance Series. Eaton SS, Eaton GR, Berliner LJ, eds, vol 23, pp 125-146. Kluwer Academic Publishers, The Netherlands, New York, Boston.
• Schneider MR, Schmidt-Ullrich R, Paus R (2009) The hair follicle as a dynamic miniorgan. Curr Biol 19: R132-R142.
• Schraermeyer U (1991) Fine structure of melanogenesis in the ink sack of Sepia officinalis. Pigment Cell Res 7: 52-60.
• Shamoto-Nagai M, Maruyama W, Yi H, Akao Y, Tribl F, Gerlach M, Osawa T, Riederer P, Naoi M (2006) Neuromelanin induces oxidative stress in mitochondria through release of iron: mechanism behind the inhibition of 26S proteasome. J Neural Transm 113: 633-644.
• Shirai A, Tsunoda H, Tamaoki T, Kamiya T (2001) Topical application of cyclosporine A induces rapid-remodeling of damaged anagen hair follicles produced in cyclophosphamide administered mice. J Dermatol Sci 27: 7-13.
• Slominski A, Paus R (1993) Melanogenesis is coupled to murine anagen: toward new concepts for the role of melanocytes and the regulation of melanogenesis in hair growth. J Invest Dermatol 101: 90S-97S.
• Slominski A, Paus R, Costantino R (1991) Differential expression and activity of melanogenesis-related proteins during induced hair growth in mice. J Invest Dermatol 96: 172-179.
• Slominski A, Paus R, Plonka P, Maurer M, Chakraborty A, Pruski D, Lukiewicz S (1994) Melanogenesis during the anagencatagen-telogen transformation of the murine hair cycle. J Invest Dermatol 102: 862-869.
• Slominski A, Goodman-Snitkoff G, Maurer M, Paus R (1997) Hair cycle-associated changes in splenocyte proliferation. In Vivo 11: 101-102.
• Slominski A, Tobin DJ, Shibahara S, Wortsman J (2004) Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol Rev 84: 1155-1228.
• Slominski A, Wortsman J, Plonka PM, Schallreuter KU, Paus R, Tobin DJ (2005) Hair follicle pigmentation. J Invest Dermatol 124: 13-21.
• Slominski A, Zbytek B, Slominski R (2009) Inhibitors of melanogenesis increase toxicity of cyclophosphamide and lymphocytes against melanoma cells. Int J Cancer 124: 1470-1477.
• Stenn KS, Paus R (2001) Controls of hair follicle cycling. Physiol Rev 81: 449-494.
• Sulaimon SS, Kitchell BE (2003) The biology of melanocytes. Vet Dermatol 14: 57-65.
• Sundberg JP (1991) Pigmented spleens in C57BL mice. Lab Anim 25: 85-86.
• Sundberg JP, King LE Jr (2000) Skin and its appendages: Normal anatomy and pathology of spontaneous, transgenic, and targeted mouse mutations. In Pathology of genetically engineered mice. Ward JM, Mahler JF, Marnopt RR, Sundberg JP, Frederickson RM, eds, pp 183-215. Iowa State University Press, Ames, IA.
• Swartz HM, Mason RP, Hogg N, Kalyanaraman B, Sarna T, Plonka PM, Zareba M, Gutierrez PL, Berliner LJ (2005) Free radicals and medicine. In Biomedical ESR. Biological Magnetic Resonance Series. Eaton SS, Eaton GR, Berliner LJ, eds, vol. 23, pp 25-74. Kluwer Academic Publishers, The Netherlands, New York, Boston.
• Tobin DJ (1998) A possible role for Langerhans cells in the removal of melanin from early catagen hair follicle. Br J Dermatol 138: 795-798.
• Tobin D J, Paus R (2001) Graying: Gerontobiology of the hair follicle pigmentary unit. Exp Gerontol 36: 29-54.
• Tobin DJ, Hagen E, Botchkarev VA, Paus R (1998) Do hair bulb melanocytes undergo apoptosis during hair follicle regression (catagen)? J Invest Dermatol 111: 941-947.
• Tobin DJ, Slominski A, Botchkarev V, Paus R (1999) The fate of hair follicle melanocytes during the hair growth cycle. J Investig Dermatol Symp Proc 4: 323-332.
• Van den Bossche K, Naeyaert J-M, Lambert J (2006) The quest for the mechanism of melanin transfer. Traffic 7: 769-778.
• Van der Heijden A, van Dijk JE, Lemmens AG, Beynen AC (1995) Spleen pigmentation in young C57BL mice is caused by accumulation of melanin. Lab Anim 29: 459-463.
• Veninga TS, Wieringa RA, Morse H (1989) Pigmented spleens in C57BL mice. Lab Anim 23: 16-20.
• Wassermann HP (1967) Extension of the concept vertebrate epidermal melanin unit to embrace visceral pigmentation and leucocytic melanin transport. Nature 213: 282-283.
• Weissman I (1967) Genetic and histochemical studies on mouse spleen black spots. Nature 215: 315.
• West JD, McLaren A (1976) The distribution of melanocytes in the dorsal coats of a series of chimaeric mice. J Embryol Exp Morphol 35: 87-93.
• Wilczok T, Stepień K, Buszman E, Porebska-Budny M (1990) Interaction of methotrexate with melanins and melanosomes from B16 melanoma. Biophys Chem 35: 265-270.
• Wulf HC, Sandby-Møller J, Kobayasi T, Gniadecki R (2004) Skin aging and natural photoprotection. Micron 35: 185-191.
• Young P, Boussadia O, Halfter H, Grose R, Berger P, Leone DP, Robenek H, Charnay P, Kemler R, Suter U (2003) E-cadherin controls adherens junctions in the epidermis and the renewal of hair follicles. EMBO J 22: 5723-5733.