Multipotent Nestin-Positive Stem Cells Reside in the Stroma of Human Eccrine and Apocrine Sweat Glands and Can Be Propagated Robustly In Vitro

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Nagel, Sabine ^a   Rohr, Franziska ^a   Weber, Caroline ^a   Kier, Janina ^a   Siemers, Frank ^b   Kruse, Charli ^a   Danner, Sandra ^a   Brandenburger, Matthias ^a   Matthiessen, Anna Emilia ^a  

^a Fraunhofer Institute for Marine Biotechnology   (Germany)

^b UNIVERSITY OF LÜBECK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA6 INTEGRIN; CYTOKINE; GROWTH RELATED ONCOGENE ALPHA; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; NESTIN; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG;

ADULT; ADULT STEM CELL; APOCRINE GLAND; ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CELL RENEWAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE RELEASE; ECTODERM; FEMALE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MALE; MULTIPOTENT STEM CELL; PILOT STUDY; PROTEIN EXPRESSION; SWEAT GLAND; SWEAT GLAND STROMA DERIVED STEM CELL; AXILLA; BIOPSY; EPIDERMIS; METABOLISM; MIDDLE AGED; PHYSIOLOGY; PROCEDURES; SKIN; YOUNG ADULT;

ADULT; APOCRINE GLANDS; AXILLA; BIOPSY; CELL DIFFERENTIATION; CYTOKINES; ECCRINE GLANDS; EPIDERMIS; FEMALE; HUMANS; MALE; MIDDLE AGED; MULTIPOTENT STEM CELLS; NESTIN; SKIN; YOUNG ADULT;

EID: 84886264719     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078365     Document Type: Article

References (77)

1. Dahlstrand J, Zimmerman LB, McKay RD, Lendahl U, (1992) Characterization of the human nestin gene reveals a close evolutionary relationship to neurofilaments. J Cell Sci 103(2):: 589-597. PubMed: 1478958.
2. Yaworsky PJ, Kappen C, (1999) Heterogeneity of neural progenitor cells revealed by enhancers in the nestin gene. Dev Biol 205: 309-321. doi:10.1006/dbio.1998.9035. PubMed: 9917366.
3. Lendahl U, Zimmerman LB, McKay RD, (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60: 585-595. doi:10.1016/0092-8674(90)90662-X. PubMed: 1689217.
4. Lothian C, Lendahl U, (1997) An evolutionarily conserved region in the second intron of the human nestin gene directs gene expression to CNS progenitor cells and to early neural crest cells. Eur J Neurosci 9: 452-462. doi:10.1111/j.1460-9568.1997.tb01622.x. PubMed: 9104587.
5. Wiese C, Rolletschek A, Kania G, Blyszczuk P, Tarasov KV, et al. (2004) Nestin expression--a property of multi-lineage progenitor cells? Cell Mol Life Sci 61: 2510-2522. doi:10.1007/s00018-004-4144-6. PubMed: 15526158.
6. Amoh Y, Li L, Katsuoka K, Hoffman RM, (2009) Multipotent nestin-expressing hair follicle stem cells. J Dermatol 36: 1-9. doi:10.1111/j.1346-8138.2008.00578.x. PubMed: 19207430.
7. Hoffman RM, (2007) The potential of nestin-expressing hair follicle stem cells in regenerative medicine. Expert Opin Biol Ther 7: 289-291. doi:10.1517/14712598.7.3.289. PubMed: 17309321.
8. Li L, Mignone J, Yang M, Matic M, Penman S, et al. (2003) Nestin expression in hair follicle sheath progenitor cells. Proc Natl Acad Sci U S A 100: 9958-9961. doi:10.1073/pnas.1733025100. PubMed: 12904579.
9. Toma JG, Akhavan M, Fernandes KJ, Barnabé-Heider F, Sadikot A, et al. (2001) Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3: 778-784. doi:10.1038/ncb0901-778. PubMed: 11533656.
10. Park D, Xiang AP, Mao FF, Zhang L, Di CG, et al. (2010) Nestin is required for the proper self-renewal of neural stem cells. Stem Cells 28: 2162-2171. doi:10.1002/stem.541. PubMed: 20963821.
11. Sahlgren CM, Mikhailov A, Hellman J, Chou YH, Lendahl U, et al. (2001) Mitotic reorganization of the intermediate filament protein nestin involves phosphorylation by cdc2 kinase. J Biol Chem 276: 16456-16463. doi:10.1074/jbc.M009669200. PubMed: 11278541.
12. Kruse C, Bodó E, Petschnik AE, Danner S, Tiede S, et al. (2006) Towards the development of a pragmatic technique for isolating and differentiating nestin-positive cells from human scalp skin into neuronal and glial cell populations: generating neurons from human skin? Exp Dermatol 15: 794-800. doi:10.1111/j.1600-0625.2006.00471.x. PubMed: 16984261.
13. Toma JG, McKenzie IA, Bagli D, Miller FD, (2005) Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 23: 727-737. doi:10.1634/stemcells.2004-0134. PubMed: 15917469.
14. Kruse C, Birth M, Rohwedel J, Assmuth, [!(surname)!], Goepel A, et al. (2004) Pluripotency of adult stem cells derived from human and rat pancreas. Appl Phys A 79: 1617-1624.
15. Gorjup E, Danner S, Rotter N, Habermann J, Brassat U, et al. (2009) Glandular tissue from human pancreas and salivary gland yields similar stem cell populations. Eur J Cell Biol 88: 409-421. doi:10.1016/j.ejcb.2009.02.187. PubMed: 19410331.
16. Petschnik AE, Klatte JE, Evers LH, Kruse C, Paus R, et al. (2010) Phenotypic indications that human sweat glands are a rich source of nestin-positive stem cell populations. Br J Dermatol 162: 380-383. doi:10.1111/j.1365-2133.2009.09512.x. PubMed: 19772523.
17. Tiede S, Kloepper JE, Ernst N, Poeggeler B, Kruse C, et al. (2009) Nestin in human skin: exclusive expression in intramesenchymal skin compartments and regulation by leptin. J Invest Dermatol 129: 2711-2720. doi:10.1038/jid.2009.148. PubMed: 19554024.
18. Amoh Y, Kanoh M, Niiyama S, Hamada Y, Kawahara K, et al. (2009) Human hair follicle pluripotent stem (hfPS) cells promote regeneration of peripheral-nerve injury: an advantageous alternative to ES and iPS cells. J Cell Biochem 107: 1016-1020. doi:10.1002/jcb.22204. PubMed: 19507228.
19. Amoh Y, Hoffman RM, (2010) Isolation and culture of hair follicle pluripotent stem (hfPS) cells and their use for nerve and spinal cord regeneration. Methods Mol Biol 585: 401-420. doi:10.1007/978-1-60761-380-0_28. PubMed: 19908019.
20. Aki R, Amoh Y, Li L, Katsuoka K, Hoffman RM, (2010) Nestin-expressing interfollicular blood vessel network contributes to skin transplant survival and wound healing. J Cell Biochem 110: 80-86. PubMed: 20225276.
21. Amoh Y, Li L, Yang M, Moossa AR, Katsuoka K, et al. (2004) Nascent blood vessels in the skin arise from nestin-expressing hair-follicle cells. Proc Natl Acad Sci U S A 101: 13291-13295. doi:10.1073/pnas.0405250101. PubMed: 15331785.
22. Danner S, Kremer M, Petschnik AE, Nagel S, Zhang Z, et al. (2012) The Use of Human Sweat Gland-Derived Stem Cells for Enhancing Vascularization during Dermal Regeneration. J Invest Dermatol 132: 1707-1716. doi:10.1038/jid.2012.31. PubMed: 22377762.
23. Biedermann T, Pontiggia L, Böttcher-Haberzeth S, Tharakan S, Braziulis E, et al. (2010) Human eccrine sweat gland cells can reconstitute a stratified epidermis. J Invest Dermatol 130: 1996-2009. doi:10.1038/jid.2010.83. PubMed: 20376062.
24. Rittié L, Sachs DL, Orringer JS, Voorhees JJ, Fisher GJ, (2012) Eccrine Sweat Glands are Major Contributors to Reepithelialization of Human Wounds. Am J Pathol 182: 163-171. PubMed: 23159944.
25. Lu CP, Polak L, Rocha AS, Pasolli HA, Chen SC, et al. (2012) Identification of stem cell populations in sweat glands and ducts reveals roles in homeostasis and wound repair. Cell 150: 136-150. doi:10.1016/j.cell.2012.04.045. PubMed: 22770217.
26. Ji KH, Xiong J, Hu KM, Fan LX, Liu HQ, (2008) Simultaneous expression of Oct4 and genes of three germ layers in single cell-derived multipotent adult progenitor cells. Ann Hematol 87: 431-438. doi:10.1007/s00277-008-0470-3. PubMed: 18338169.
27. Chambers I, Colby D, Robertson M, Nichols J, Lee S, et al. (2003) Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113: 643-655. doi:10.1016/S0092-8674(03)00392-1. PubMed: 12787505.
28. Ernst N, Tiede S, Tronnier V, Kruse C, Zechel C, et al. (2010) An improved, standardised protocol for the isolation, enrichment and targeted neural differentiation of Nestin+ progenitors from adult human dermis. Exp Dermatol 19: 549-555. doi:10.1111/j.1600-0625.2009.01041.x. PubMed: 20100195.
29. Ersch J, Stallmach T, (1999) Assessing gestational age from histology of fetal skin: an autopsy study of 379 fetuses. Obstet Gynecol 94: 753-757. doi:10.1016/S0029-7844(99)00379-8. PubMed: 10546723.
30. Holbrook KA, Minami SI, (1991) Hair follicle embryogenesis in the human. Characterization of events in vivo and in vitro. Ann N Y Acad Sci 642: 167-196. PubMed: 1809080.
31. Moll I, Moll R, (1992) Changes of expression of intermediate filament proteins during ontogenesis of eccrine sweat glands. J Invest Dermatol 98: 777-785. doi:10.1111/1523-1747.ep12499950. PubMed: 1569327.
32. Cowin P, Wysolmerski J, (2010) Molecular mechanisms guiding embryonic mammary gland development. Cold Spring Harb Perspect Biol 2: a003251. doi:10.1101/cshperspect.a003251. PubMed: 20484386.
33. Li H, Cherukuri P, Li N, Cowling V, Spinella M, et al. (2007) Nestin is expressed in the basal/myoepithelial layer of the mammary gland and is a selective marker of basal epithelial breast tumors. Cancer Res 67: 501-510. doi:10.1158/0008-5472.CAN-05-4571. PubMed: 17234757.
34. Kolar Z, Ehrmann J Jr., Turashvili G, Bouchal J, Mokry J, (2007) A novel myoepithelial/progenitor cell marker in the breast? Virchows Arch 450: 607-609. doi:10.1007/s00428-007-0403-x. PubMed: 17429688.
35. Rapoport DH, Schicktanz S, Gürleyik E, Zühlke C, Kruse C, (2009) Isolation and in vitro cultivation turns cells from exocrine human pancreas into multipotent stem-cells. Ann Anat 191: 446-458. doi:10.1016/j.aanat.2009.07.002. PubMed: 19716277.
36. Fong H, Hohenstein KA, Donovan PJ, (2008) Regulation of self-renewal and pluripotency by Sox2 in human embryonic stem cells. Stem Cells 26: 1931-1938. doi:10.1634/stemcells.2007-1002. PubMed: 18388306.
37. Reubinoff BE, Pera MF, Fong CY, Trounson A, Bongso A, (2000) Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol 18: 399-404. doi:10.1038/74447. PubMed: 10748519.
38. Schöler HR, Ruppert S, Suzuki N, Chowdhury K, Gruss P, (1990) New type of POU domain in germ line-specific protein Oct-4. Nature 344: 435-439. doi:10.1038/344435a0. PubMed: 1690859.
39. Tai MH, Chang CC, Kiupel M, Webster JD, Olson LK, et al. (2005) Oct4 expression in adult human stem cells: evidence in support of the stem cell theory of carcinogenesis. Carcinogenesis 26: 495-502. PubMed: 15513931.
40. Yu H, Fang D, Kumar SM, Li L, Nguyen TK, et al. (2006) Isolation of a novel population of multipotent adult stem cells from human hair follicles. Am J Pathol 168: 1879-1888. doi:10.2353/ajpath.2006.051170. PubMed: 16723703.
41. Yang C, Zhu P, Yan L, Chen L, Meng R, et al. (2009) Dynamic changes in matrix metalloproteinase 9 and tissue inhibitor of metalloproteinase 1 levels during wound healing in diabetic rats. J Am Podiatr Med Assoc 99: 489-496. PubMed: 19917734.
42. Distler JH, Hirth A, Kurowska-Stolarska M, Gay RE, Gay S, et al. (2003) Angiogenic and angiostatic factors in the molecular control of angiogenesis. Q J Nucl Med 47: 149-161. PubMed: 12897707.
43. Werner S, Grose R, (2003) Regulation of wound healing by growth factors and cytokines. Physiol Rev 83: 835-870. PubMed: 12843410.
44. Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M, (2008) Growth factors and cytokines in wound healing. Wound Repair Regen 16: 585-601. doi:10.1111/j.1524-475X.2008.00410.x. PubMed: 19128254.
45. Gurtner GC, Werner S, Barrandon Y, Longaker MT, (2008) Wound repair and regeneration. Nature 453: 314-321. doi:10.1038/nature07039. PubMed: 18480812.
46. Sinha S, Fuchs E, (2001) Identification and dissection of an enhancer controlling epithelial gene expression in skin. Proc Natl Acad Sci U_S_A 98: 2455-2460. doi:10.1073/pnas.051633598. PubMed: 11226260.
47. Gho CG, Braun JE, Tilli CM, Neumann HA, Ramaekers FC, (2004) Human follicular stem cells: their presence in plucked hair and follicular cell culture. Br J Dermatol 150: 860-868. doi:10.1111/j.1365-2133.2004.05862.x. PubMed: 15149497.
48. Purkis PE, Steel JB, Mackenzie IC, Nathrath WB, Leigh IM, et al. (1990) Antibody markers of basal cells in complex epithelia. J Cell Sci 97(1):: 39-50. PubMed: 1701769.
49. Pontiggia L, Biedermann T, Meuli M, Widmer D, Böttcher-Haberzeth S, et al. (2009) Markers to evaluate the quality and self-renewing potential of engineered human skin substitutes in vitro and after transplantation. J Invest Dermatol 129: 480-490. doi:10.1038/jid.2008.254. PubMed: 18719609.
50. Cotsarelis G, (2006) Epithelial stem cells: a folliculocentric view. J Invest Dermatol 126: 1459-1468. doi:10.1038/sj.jid.5700376. PubMed: 16778814.
51. Akiyama M, Smith LT, Shimizu H, (2000) Changing patterns of localization of putative stem cells in developing human hair follicles. J Invest Dermatol 114: 321-327. doi:10.1046/j.1523-1747.2000.00857.x. PubMed: 10651993.
52. Larouche D, Hayward C, Cuffley K, Germain L, (2005) Keratin 19 as a stem cell marker in vivo and in vitro. Methods Mol Biol 289: 103-110. PubMed: 15502175.
53. Kloepper JE, Tiede S, Brinckmann J, Reinhardt DP, Meyer W, et al. (2008) Immunophenotyping of the human bulge region: the quest to define useful in situ markers for human epithelial hair follicle stem cells and their niche. Exp Dermatol 17: 592-609. doi:10.1111/j.1600-0625.2008.00720.x. PubMed: 18558994.
54. Bouvard C, Gafsou B, Dizier B, Galy-Fauroux I, Lokajczyk A, et al. (2010) alpha6-integrin subunit plays a major role in the proangiogenic properties of endothelial progenitor cells. Arterioscler Thromb Vasc Biol 30: 1569-1575. doi:10.1161/ATVBAHA.110.209163. PubMed: 20508204.
55. Chung J, Bachelder RE, Lipscomb EA, Shaw LM, Mercurio AM, (2002) Integrin (alpha 6 beta 4) regulation of eIF-4E activity and VEGF translation: a survival mechanism for carcinoma cells. J Cell Biol 158: 165-174. doi:10.1083/jcb.200112015. PubMed: 12105188.
56. Spradling A, Drummond-Barbosa D, Kai T, (2001) Stem cells find their niche. Nature 414: 98-104. doi:10.1038/35102160. PubMed: 11689954.
57. Yu KR, Yang SR, Jung JW, Kim H, Ko K, et al. (2012) CD49f enhances multipotency and maintains stemness through the direct regulation of OCT4 and SOX2. Stem Cells 30: 876-887. doi:10.1002/stem.1052. PubMed: 22311737.
58. Carroll DK, Carroll JS, Leong CO, Cheng F, Brown M, et al. (2006) p63 regulates an adhesion programme and cell survival in epithelial cells. Nat Cell Biol 8: 551-561. doi:10.1038/ncb1420. PubMed: 16715076.
59. Schreder A, Pierard GE, Paquet P, Reginster MA, Pierard-Franchimont C, et al. (2010) Facing towards epidermal stem cells (Review). Int J Mol Med 26: 171-174 PubMed: 20596595.
60. Senoo M, Pinto F, Crum CP, McKeon F, (2007) p63 Is essential for the proliferative potential of stem cells in stratified epithelia. Cell 129: 523-536. doi:10.1016/j.cell.2007.02.045. PubMed: 17482546.
61. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, et al. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147. doi:10.1126/science.284.5411.143. PubMed: 10102814.
62. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, et al. (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418: 41-49. doi:10.1038/nature00870. PubMed: 12077603.
63. Eliasson C, Sahlgren C, Berthold CH, Stakeberg J, Celis JE, et al. (1999) Intermediate filament protein partnership in astrocytes. J Biol Chem 274: 23996-24006. doi:10.1074/jbc.274.34.23996. PubMed: 10446168.
64. Mokrý J, Ehrmann J, Karbanová J, Cízková D, Soukup T, et al. (2008) Expression of intermediate filament nestin in blood vessels of neural and non-neural tissues. Acta Med (Hradec Kralove) 51: 173-179. PubMed: 19271685.
65. Schmidt A, Ladage D, Schinköthe T, Klausmann U, Ulrichs C, et al. (2006) Basic fibroblast growth factor controls migration in human mesenchymal stem cells. Stem Cells 24: 1750-1758. doi:10.1634/stemcells.2005-0191. PubMed: 16822883.
66. Steinert PM, Chou YH, Prahlad V, Parry DA, Marekov LN, et al. (1999) A high molecular weight intermediate filament-associated protein in BHK-21 cells is nestin, a type VI intermediate filament protein. Limited co-assembly in vitro to form heteropolymers with type III vimentin and type IV alpha-internexin. J Biol Chem 274: 9881-9890. doi:10.1074/jbc.274.14.9881. PubMed: 10092680.
67. Chou YH, Khuon S, Herrmann H, Goldman RD, (2003) Nestin promotes the phosphorylation-dependent disassembly of vimentin intermediate filaments during mitosis. Mol Cell Biol 14: 1468-1478. doi:10.1091/mbc.E02-08-0545. PubMed: 12686602.
68. Chang L, Goldman RD, (2004) Intermediate filaments mediate cytoskeletal crosstalk. Nat Rev Mol Cell Biol 5: 601-613. doi:10.1038/nrm1438. PubMed: 15366704.
69. Fernandes KJ, McKenzie IA, Mill P, Smith KM, Akhavan M, et al. (2004) A dermal niche for multipotent adult skin-derived precursor cells. Nat Cell Biol 6: 1082-1093. doi:10.1038/ncb1181. PubMed: 15517002.
70. Sieber-Blum M, Grim M, (2004) The adult hair follicle: cradle for pluripotent neural crest stem cells. Birth Defects Res C Embryo TODAY 72: 162-172. doi:10.1002/bdrc.20008. PubMed: 15269890.
71. Wong CE, Paratore C, Dours-Zimmermann MT, Rochat A, Pietri T, et al. (2006) Neural crest-derived cells with stem cell features can be traced back to multiple lineages in the adult skin. J Cell Biol 175: 1005-1015. doi:10.1083/jcb.200606062. PubMed: 17158956.
72. Aihara M, Sugawara K, Torii S, Hosaka M, Kurihara H, et al. (2004) Angiogenic endothelium-specific nestin expression is enhanced by the first intron of the nestin gene. Lab Invest 84: 1581-1592. doi:10.1038/labinvest.3700186. PubMed: 15502861.
73. Mokrý J, Cízková D, Filip S, Ehrmann J, Osterreicher J, et al. (2004) Nestin expression by newly formed human blood vessels. Stem Cells Dev 13: 658-664. doi:10.1089/scd.2004.13.658. PubMed: 15684833.
74. Kim DS, Cho HJ, Choi HR, Kwon SB, Park KC, (2004) Isolation of human epidermal stem cells by adherence and the reconstruction of skin equivalents. Cell Mol Life Sci 61: 2774-2781. doi:10.1007/s00018-004-4288-4. PubMed: 15549181.
75. Petschnik AE, Fell B, Tiede S, Habermann JK, Pries R, et al. (2011) A novel xenogeneic co-culture system to examine neuronal differentiation capability of various adult human stem cells. PLOS ONE 6: e24944. doi:10.1371/journal.pone.0024944. PubMed: 21935488.
76. Jaiswal N, Haynesworth SE, Caplan AI, Bruder SP, (1997) Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 64: 295-312. doi:10.1002/(SICI)1097-4644(199702)64:2. PubMed: 9027589.
77. Mackay AM, Beck SC, Murphy JM, Barry FP, Chichester CO, et al. (1998) Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 4: 415-428. doi:10.1089/ten.1998.4.415. PubMed: 9916173.