Melanocyte stem cells as potential therapeutics in skin disorders

Bibliography

• Randhawa M, Huff T, Valencia JC, et al. Evidence for the ectopic synthesis of melanin in human adipose tissue. FASEB J 2009;23(3):835-43
   PubMed Web of Science ®Google Scholar
• Dupin E, Sommer L. Neural crest progenitors and stem cells: from early development to adulthood. Dev Biol 2012;366(1):83-95
   PubMed Web of Science ®Google Scholar
• Yaar M, Park HY. Melanocytes: a window into the nervous system. J Invest Dermatol 2012;132(3 Pt 2):835-45
   PubMed Web of Science ®Google Scholar
• Wittgen HG, van Kempen LC. Reactive oxygen species in melanoma and its therapeutic implications. Melanoma Res 2007;17(6):400-9
   PubMed Web of Science ®Google Scholar
• Funasaka Y, Komoto M, Ichihashi M. Depigmenting effect of alpha-tocopheryl ferulate on normal human melanocytes. Pigment Cell Res 2000;13(Suppl 8):170-4
   PubMedGoogle Scholar
• Slominski A, Wortsman J, Tobin DJ. The cutaneous serotoninergic/melatoninergic system: securing a place under the sun. FASEB J 2005;19(2):176-94
   PubMed Web of Science ®Google Scholar
• Slominski AT, Zmijewski MA, Skobowiat C, et al. Sensing the environment: regulation of local and global homeostasis by the skin’s neuroendocrine system. Adv Anat Embryol Cell Biol 2012;212:v, vii, 1-115
   Google Scholar
• Slominski AT, Zmijewski MA, Zbytek B, et al. Key role of CRF in the skin stress response system. Endocr Rev 2013;34(6):827-84
   PubMed Web of Science ®Google Scholar
• Slominski A, Wortsman J, Luger T, et al. Corticotropin releasing hormone and proopiomelanocortin involvement in the cutaneous response to stress. Physiol Rev 2000;80(3):979-1020
   PubMed Web of Science ®Google Scholar
• Slominski A, Zbytek B, Nikolakis G, et al. Steroidogenesis in the skin: implications for local immune functions. J Steroid Biochem Mol Biol 2013;137:107-23
   PubMed Web of Science ®Google Scholar
• Le Douarin NM, Creuzet S, Couly G, Dupin E. Neural crest cell plasticity and its limits. Development 2004;131(19):4637-50
   PubMed Web of Science ®Google Scholar
• Weston JA. The migration and differentiation of neural crest cells. Adv Morphog 1970;8:41-114
   PubMedGoogle Scholar
• Ernfors P. Cellular origin and developmental mechanisms during the formation of skin melanocytes. Exp Cell Res 2010;316(8):1397-407
   PubMed Web of Science ®Google Scholar
• Slominski A, Paus R, Schadendorf D. Melanocytes as "sensory" and regulatory cells in the epidermis. J Theor Biol 1993;164(1):103-20
   PubMed Web of Science ®Google Scholar
• Dupin E, Le Douarin NM. Development of melanocyte precursors from the vertebrate neural crest. Oncogene 2003;22(20):3016-23
   PubMed Web of Science ®Google Scholar
• Dupin E, Real C, Glavieux-Pardanaud C, et al. Reversal of developmental restrictions in neural crest lineages: transition from Schwann cells to glial-melanocytic precursors in vitro. Proc Natl Acad Sci USA 2003;100(9):5229-33
   PubMed Web of Science ®Google Scholar
• Adameyko I, Lallemend F, Aquino JB, et al. Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell 2009;139(2):366-79
   PubMed Web of Science ®Google Scholar
• Kawakami T, Kumasaka M, Kato M, et al. BMP-4 down-regulates the expression of Ret in murine melanocyte precursors. J Dermatol Sci 2011;63(1):66-9
   PubMed Web of Science ®Google Scholar
• Gleason BC, Crum CP, Murphy GF. Expression patterns of MITF during human cutaneous embryogenesis: evidence for bulge epithelial expression and persistence of dermal melanoblasts. J Cutan Pathol 2008;35(7):615-22
   PubMed Web of Science ®Google Scholar
• Motohashi T, Yamanaka K, Chiba K, et al. Unexpected multipotency of melanoblasts isolated from murine skin. Stem Cells 2009;27(4):888-97
   PubMed Web of Science ®Google Scholar
• Sommer L. Checkpoints of melanocyte stem cell development. Sci STKE 2005;2005(298):pe42
   PubMedGoogle Scholar
• Trentin A, Glavieux-Pardanaud C, Le Douarin NM, Dupin E. Self-renewal capacity is a widespread property of various types of neural crest precursor cells. Proc Natl Acad Sci USA 2004;101(13):4495-500
   PubMed Web of Science ®Google Scholar
• Slominski A, Wortsman J. Neuroendocrinology of the skin. Endocr Rev 2000;21(5):457-87
   PubMed Web of Science ®Google Scholar
• Slominski A, Wortsman J, Plonka PM, et al. Hair follicle pigmentation. J Invest Dermatol 2005;124(1):13-21
   PubMed Web of Science ®Google Scholar
• Van Den Bossche K, Naeyaert JM, Lambert J. The quest for the mechanism of melanin transfer. Traffic 2006;7(7):769-78
   PubMed Web of Science ®Google Scholar
• Slominski A, Paus R. 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 1993;101(1 Suppl):90S-7S
   PubMed Web of Science ®Google Scholar
• Slominski A, Tobin DJ, Shibahara S, Wortsman J. Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol Rev 2004;84(4):1155-228
   PubMed Web of Science ®Google Scholar
• Slominski A, Paus R, Costantino R. Differential expression and activity of melanogenesis-related proteins during induced hair growth in mice. J Invest Dermatol 1991;96(2):172-9
   PubMed Web of Science ®Google Scholar
• Slominski A, Paus R, Plonka P, et al. Melanogenesis during the anagen-catagen-telogen transformation of the murine hair cycle. J Invest Dermatol 1994;102(6):862-9
   PubMed Web of Science ®Google Scholar
• Slominski A, Paus R, Plonka P, et al. Pharmacological disruption of hair follicle pigmentation by cyclophosphamide as a model for studying the melanocyte response to and recovery from cytotoxic drug damage in situ. J Invest Dermatol 1996;106(6):1203-11
   PubMed Web of Science ®Google Scholar
• Widlund HR, Fisher DE. Microphthalamia-associated transcription factor: a critical regulator of pigment cell development and survival. Oncogene 2003;22(20):3035-41
   PubMed Web of Science ®Google Scholar
• Lin CB, Babiarz L, Liebel F, et al. Modulation of microphthalmia-associated transcription factor gene expression alters skin pigmentation. J Invest Dermatol 2002;119(6):1330-40
   PubMed Web of Science ®Google Scholar
• Fisher DE. Microphthalmia: a signal responsive transcriptional regulator in development. Pigment Cell Res 2000;13(Suppl 8):145-9
   PubMedGoogle Scholar
• Hemesath TJ, Steingrimsson E, McGill G, et al. microphthalmia, a critical factor in melanocyte development, defines a discrete transcription factor family. Genes Dev 1994;8(22):2770-80
   PubMed Web of Science ®Google Scholar
• Tabone-Eglinger S, Wehrle-Haller M, Aebischer N, et al. Membrane-bound Kit ligand regulates melanocyte adhesion and survival, providing physical interaction with an intraepithelial niche. FASEB J 2012;26(9):3738-53
   PubMed Web of Science ®Google Scholar
• Peters EM, Tobin DJ, Botchkareva N, et al. Migration of melanoblasts into the developing murine hair follicle is accompanied by transient c-Kit expression. J Histochem Cytochem 2002;50(6):751-66
   PubMed Web of Science ®Google Scholar
• Mackenzie MA, Jordan SA, Budd PS, Jackson IJ. Activation of the receptor tyrosine kinase Kit is required for the proliferation of melanoblasts in the mouse embryo. Dev Biol 1997;192(1):99-107
   PubMed Web of Science ®Google Scholar
• Opdecamp K, Nakayama A, Nguyen MT, et al. Melanocyte development in vivo and in neural crest cell cultures: crucial dependence on the Mitf basic-helix-loop-helix-zipper transcription factor. Development 1997;124(12):2377-86
   PubMed Web of Science ®Google Scholar
• Steel KP, Davidson DR, Jackson IJ. TRP-2/DT, a new early melanoblast marker, shows that steel growth factor (c-kit ligand) is a survival factor. Development 1992;115(4):1111-19
   PubMed Web of Science ®Google Scholar
• Slominski A, Zmijewski MA, Pawelek J. L-tyrosine and L-dihydroxyphenylalanine as hormone-like regulators of melanocyte functions. Pigment Cell Melanoma Res 2012;25(1):14-27
   PubMed Web of Science ®Google Scholar
• Nishimura EK, Jordan SA, Oshima H, et al. Dominant role of the niche in melanocyte stem-cell fate determination. Nature 2002;416(6883):854-60
   PubMed Web of Science ®Google Scholar
• Osawa M, Egawa G, Mak SS, et al. Molecular characterization of melanocyte stem cells in their niche. Development 2005;132(24):5589-99
   PubMed Web of Science ®Google Scholar
• Nishikawa SI, Osawa M, Yonetani S, et al. Niche required for inducing quiescent stem cells. Cold Spring Harb Symp Quant Biol 2008;73:67-71
   PubMedGoogle Scholar
• Nishikawa S, Osawa M. Generating quiescent stem cells. Pigment Cell Res 2007;20(4):263-70
   PubMedGoogle Scholar
• Freter R, Osawa M, Nishikawa S. Adult stem cells exhibit global suppression of RNA polymerase II serine-2 phosphorylation. Stem Cells 2010;28(9):1571-80
   PubMed Web of Science ®Google Scholar
• Nishimura EK, Granter SR, Fisher DE. Mechanisms of hair graying: incomplete melanocyte stem cell maintenance in the niche. Science 2005;307(5710):720-4
   PubMed Web of Science ®Google Scholar
• Nishimura EK, Suzuki M, Igras V, et al. Key roles for transforming growth factor beta in melanocyte stem cell maintenance. Cell Stem Cell 2010;6(2):130-40
   PubMed Web of Science ®Google Scholar
• Blanpain C, Sotiropoulou PA. A dominant role of the hair follicle stem cell niche in regulating melanocyte stemness. Cell Stem Cell 2010;6(2):95-6
   PubMed Web of Science ®Google Scholar
• Sharov A, Tobin DJ, Sharova TY, et al. Changes in different melanocyte populations during hair follicle involution (catagen). J Invest Dermatol 2005;125(6):1259-67
   PubMed Web of Science ®Google Scholar
• Tobin DJ, Hagen E, Botchkarev VA, Paus R. Do hair bulb melanocytes undergo apoptosis during hair follicle regression (catagen)? J Invest Dermatol 1998;111(6):941-7
   PubMed Web of Science ®Google Scholar
• Myung P, Ito M. Dissecting the bulge in hair regeneration. J Clin Invest 2012;122(2):448-54
   PubMed Web of Science ®Google Scholar
• Tobin DJ, Slominski A, Botchkarev V, Paus R. The fate of hair follicle melanocytes during the hair growth cycle. J Investig Dermatol Symp Proc 1999;4(3):323-32
   PubMed Web of Science ®Google Scholar
• Horikawa T, Norris DA, Johnson TW, et al. DOPA-negative melanocytes in the outer root sheath of human hair follicles express premelanosomal antigens but not a melanosomal antigen or the melanosome-associated glycoproteins tyrosinase, TRP-1, and TRP-2. J Invest Dermatol 1996;106(1):28-35
   PubMed Web of Science ®Google Scholar
• Narisawa Y, Kohda H, Tanaka T. Three-dimensional demonstration of melanocyte distribution of human hair follicles: special reference to the bulge area. Acta Derm Venereol 1997;77(2):97-101
   PubMed Web of Science ®Google Scholar
• Commo S, Bernard BA. Melanocyte subpopulation turnover during the human hair cycle: an immunohistochemical study. Pigment Cell Res 2000;13(4):253-9
   PubMedGoogle Scholar
• Nishikawa-Torikai S, Nishikawa S. Stem cell niche: from concept to reality. Pigment Cell Melanoma Res 2012;25(2):122-3
   PubMed Web of Science ®Google Scholar
• Yusuf I, Fruman DA. Regulation of quiescence in lymphocytes. Trends Immunol 2003;24(7):380-6
   PubMed Web of Science ®Google Scholar
• Hou L, Pavan WJ. Transcriptional and signaling regulation in neural crest stem cell-derived melanocyte development: do all roads lead to Mitf? Cell Res 2008;18(12):1163-76
   PubMed Web of Science ®Google Scholar
• Robinson KC, Fisher DE. Specification and loss of melanocyte stem cells. Semin Cell Dev Biol 2009;20(1):111-16
   PubMed Web of Science ®Google Scholar
• Uong A, Zon LI. Melanocytes in development and cancer. J Cell Physiol 2010;222(1):38-41
   PubMed Web of Science ®Google Scholar
• Pshenichnaya I, Schouwey K, Armaro M, et al. Constitutive gray hair in mice induced by melanocyte-specific deletion of c-Myc. Pigment Cell Melanoma Res 2012;25(3):312-25
   PubMed Web of Science ®Google Scholar
• McGill GG, Horstmann M, Widlund HR, et al. Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell 2002;109(6):707-18
   PubMed Web of Science ®Google Scholar
• Mak SS, Moriyama M, Nishioka E, et al. Indispensable role of Bcl2 in the development of the melanocyte stem cell. Dev Biol 2006;291(1):144-53
   PubMed Web of Science ®Google Scholar
• Yamamura K, Kamada S, Ito S, et al. Accelerated disappearance of melanocytes in bcl-2-deficient mice. Cancer Res 1996;56(15):3546-50
   PubMed Web of Science ®Google Scholar
• Steingrimsson E, Copeland NG, Jenkins NA. Melanocyte stem cell maintenance and hair graying. Cell 2005;121(1):9-12
   PubMed Web of Science ®Google Scholar
• Wellbrock C, Ogilvie L, Hedley D, et al. V599EB-RAF is an oncogene in melanocytes. Cancer Res 2004;64(7):2338-42
   PubMed Web of Science ®Google Scholar
• Heidorn SJ, Milagre C, Whittaker S, et al. Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 2010;140(2):209-21
   PubMed Web of Science ®Google Scholar
• Valluet A, Druillennec S, Barbotin C, et al. B-Raf and C-Raf are required for melanocyte stem cell self-maintenance. Cell Rep 2012;2(4):774-80
   Google Scholar
• Rabbani P, Takeo M, Chou W, et al. Coordinated activation of Wnt in epithelial and melanocyte stem cells initiates pigmented hair regeneration. Cell 2011;145(6):941-55
   PubMed Web of Science ®Google Scholar
• Tanimura S, Tadokoro Y, Inomata K, et al. Hair follicle stem cells provide a functional niche for melanocyte stem cells. Cell Stem Cell 2011;8(2):177-87
   PubMed Web of Science ®Google Scholar
• Kubic JD, Young KP, Plummer RS, et al. Pigmentation PAX-ways: the role of Pax3 in melanogenesis, melanocyte stem cell maintenance, and disease. Pigment Cell Melanoma Res 2008;21(6):627-45
   PubMed Web of Science ®Google Scholar
• Lang D, Lu MM, Huang L, et al. Pax3 functions at a nodal point in melanocyte stem cell differentiation. Nature 2005;433(7028):884-7
   PubMed Web of Science ®Google Scholar
• Tumbar T, Guasch G, Greco V, et al. Defining the epithelial stem cell niche in skin. Science 2004;303(5656):359-63
   PubMed Web of Science ®Google Scholar
• Moriyama M, Osawa M, Mak SS, et al. Notch signaling via Hes1 transcription factor maintains survival of melanoblasts and melanocyte stem cells. J Cell Biol 2006;173(3):333-9
   PubMed Web of Science ®Google Scholar
• Schouwey K, Delmas V, Larue L, et al. Notch1 and Notch2 receptors influence progressive hair graying in a dose-dependent manner. Dev Dyn 2007;236(1):282-9
   PubMed Web of Science ®Google Scholar
• Osawa M, Fisher DE. Notch and melanocytes: diverse outcomes from a single signal. J Invest Dermatol 2008;128(11):2571-4
   PubMed Web of Science ®Google Scholar
• Das AV, James J, Zhao X, et al. Identification of c-Kit receptor as a regulator of adult neural stem cells in the mammalian eye: interactions with Notch signaling. Dev Biol 2004;273(1):87-105
   PubMed Web of Science ®Google Scholar
• Chang CY, Pasolli HA, Giannopoulou EG, et al. NFIB is a governor of epithelial-melanocyte stem cell behaviour in a shared niche. Nature 2013;495(7439):98-102
   PubMed Web of Science ®Google Scholar
• Taieb A, Picardo M. The definition and assessment of vitiligo: a consensus report of the Vitiligo European Task Force. Pigment Cell Res 2007;20(1):27-35
   PubMedGoogle Scholar
• Nath SK, Majumder PP, Nordlund JJ. Genetic epidemiology of vitiligo: multilocus recessivity cross-validated. Am J Hum Genet 1994;55(5):981-90
   PubMed Web of Science ®Google Scholar
• Halder RM, Chappell JL. Vitiligo update. Semin Cutan Med Surg 2009;28(2):86-92
   PubMed Web of Science ®Google Scholar
• Nishimura EK. Melanocyte stem cells: a melanocyte reservoir in hair follicles for hair and skin pigmentation. Pigment Cell Melanoma Res 2011;24(3):401-10
   PubMed Web of Science ®Google Scholar
• Kunisada T, Lu SZ, Yoshida H, et al. Murine cutaneous mastocytosis and epidermal melanocytosis induced by keratinocyte expression of transgenic stem cell factor. J Exp Med 1998;187(10):1565-73
   PubMed Web of Science ®Google Scholar
• Tobin DJ, Swanson NN, Pittelkow MR, et al. Melanocytes are not absent in lesional skin of long duration vitiligo. J Pathol 2000;191(4):407-16
   PubMed Web of Science ®Google Scholar
• Seleit I, Bakry OA, Abdou AG, Dawoud NM. Immunohistochemical Study of Melanocyte-Melanocyte Stem Cell lineage in Vitiligo; A Clue to Interfollicular Melanocyte Stem Cell Reservoir. Ultrastruct Pathol 2014;38(3):186-98
   PubMed Web of Science ®Google Scholar
• Parsad D, Pandhi R, Dogra S, Kumar B. Clinical study of repigmentation patterns with different treatment modalities and their correlation with speed and stability of repigmentation in 352 vitiliginous patches. J Am Acad Dermatol 2004;50(1):63-7
   PubMed Web of Science ®Google Scholar
• Westerhof W, Nieuweboer-Krobotova L. Treatment of vitiligo with UV-B radiation vs topical psoralen plus UV-A. Arch Dermatol 1997;133(12):1525-8
   PubMed Web of Science ®Google Scholar
• Dong D, Jiang M, Xu X, et al. The effects of NB-UVB on the hair follicle-derived neural crest stem cells differentiating into melanocyte lineage in vitro. J Dermatol Sci 2012;66(1):20-8
   PubMed Web of Science ®Google Scholar
• Yamada T, Hasegawa S, Inoue Y, et al. Wnt/beta-catenin and kit signaling sequentially regulate melanocyte stem cell differentiation in UVB-induced epidermal pigmentation. J Invest Dermatol 2013;133(12):2753-62
   PubMed Web of Science ®Google Scholar
• Sethi S, Mahajan BB, Gupta RR, Ohri A. Comparative evaluation of the therapeutic efficacy of dermabrasion, dermabrasion combined with topical 5% 5-fluorouracil cream, and dermabrasion combined with topical placentrex gel in localized stable vitiligo. Int J Dermatol 2007;46(8):875-9
   PubMed Web of Science ®Google Scholar
• Esmat SM, El-Tawdy AM, Hafez GA, et al. Acral lesions of vitiligo: why are they resistant to photochemotherapy? J Eur Acad Dermatol Venereol 2012;26(9):1097-104
   PubMed Web of Science ®Google Scholar
• Vanscheidt W, Hunziker T. Repigmentation by outer-root-sheath-derived melanocytes: proof of concept in vitiligo and leucoderma. Dermatology 2009;218(4):342-3
   PubMed Web of Science ®Google Scholar
• Mohanty S, Kumar A, Dhawan J, et al. Noncultured extracted hair follicle outer root sheath cell suspension for transplantation in vitiligo. Br J Dermatol 2011;164(6):1241-6
   PubMed Web of Science ®Google Scholar
• Chou WC, Takeo M, Rabbani P, et al. Direct migration of follicular melanocyte stem cells to the epidermis after wounding or UVB irradiation is dependent on Mc1r signaling. Nat Med 2013;19(7):924-9
   PubMed Web of Science ®Google Scholar
• Stanley JR. Synergy of understanding dermatologic disease and epidermal biology. J Clin Invest 2012;122(2):436-9
   PubMed Web of Science ®Google Scholar
• Inomata K, Aoto T, Binh NT, et al. Genotoxic stress abrogates renewal of melanocyte stem cells by triggering their differentiation. Cell 2009;137(6):1088-99
   PubMed Web of Science ®Google Scholar
• Fuchs E. Skin stem cells: rising to the surface. J Cell Biol 2008;180(2):273-84
   PubMed Web of Science ®Google Scholar
• Nishikawa-Torikai S, Osawa M, Nishikawa S. Functional characterization of melanocyte stem cells in hair follicles. J Invest Dermatol 2011;131(12):2358-67
   PubMed Web of Science ®Google Scholar
• Falabella R, Barona MI. Update on skin repigmentation therapies in vitiligo. Pigment Cell Melanoma Res 2009;22(1):42-65
   PubMed Web of Science ®Google Scholar
• Lerner AB, Halaban R, Klaus SN, Moellmann GE. Transplantation of human melanocytes. J Invest Dermatol 1987;89(3):219-24
   PubMed Web of Science ®Google Scholar
• Olsson MJ, Juhlin L. Melanocyte transplantation in vitiligo. Lancet 1992;340(8825):981
   PubMed Web of Science ®Google Scholar
• Budania A, Parsad D, Kanwar AJ, Dogra S. Comparison between autologous noncultured epidermal cell suspension and suction blister epidermal grafting in stable vitiligo: a randomized study. Br J Dermatol 2012;167(6):1295-301
   PubMed Web of Science ®Google Scholar
• Singh C, Parsad D, Kanwar AJ, et al. Comparison between autologous noncultured extracted hair follicle outer root sheath cell suspension and autologous noncultured epidermal cell suspension in the treatment of stable vitiligo: a randomized study. Br J Dermatol 2013;169(2):287-93
   PubMed Web of Science ®Google Scholar
• Chen YF, Yang PY, Hu DN, et al. Treatment of vitiligo by transplantation of cultured pure melanocyte suspension: analysis of 120 cases. J Am Acad Dermatol 2004;51(1):68-74
   PubMed Web of Science ®Google Scholar
• Olsson MJ, Juhlin L. Transplantation of melanocytes in vitiligo. Br J Dermatol 1995;132(4):587-91
   PubMed Web of Science ®Google Scholar
• Biernaskie J. Human hair follicles: "bulging" with neural crest-like stem cells. J Invest Dermatol 2010;130(5):1202-4
   PubMed Web of Science ®Google Scholar
• Savkovic V, Dieckmann C, Milkova L, Simon JC. Improved method of differentiation, selection and amplification of human melanocytes from the hair follicle cell pool. Exp Dermatol 2012;21(12):948-50
   PubMed Web of Science ®Google Scholar
• Dieckmann C, Milkova L, Hunziker T, et al. Human melanocytes can be isolated, propagated and expanded from plucked anagen hair follicles. Exp Dermatol 2010;19(6):543-5
   PubMed Web of Science ®Google Scholar
• Ohta S, Imaizumi Y, Okada Y, et al. Generation of human melanocytes from induced pluripotent stem cells. PLoS One 2011;6(1):e16182
   PubMedGoogle Scholar
• Kinsler VA, Anderson G, Latimer B, et al. Immunohistochemical and ultrastructural features of congenital melanocytic naevus cells support a stem-cell phenotype. Br J Dermatol 2013;169(2):374-83
   PubMed Web of Science ®Google Scholar
• Veis DJ, Sorenson CM, Shutter JR, Korsmeyer SJ. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 1993;75(2):229-40
   PubMed Web of Science ®Google Scholar
• Kamada S, Shimono A, Shinto Y, et al. bcl-2 deficiency in mice leads to pleiotropic abnormalities: accelerated lymphoid cell death in thymus and spleen, polycystic kidney, hair hypopigmentation, and distorted small intestine. Cancer Res 1995;55(2):354-9
   PubMed Web of Science ®Google Scholar