Divide and conquer: two stem cell populations in squamous epithelia, reserves and the active duty forces

Spencer Dunaway , Alexandra Rothaus , Yuhang Zhang , Ana Luisa Kadekaro , Thomas Andl , Claudia D. Andl

International Journal of Oral Science ›› 2019, Vol. 11 ›› Issue (3) : 26

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International Journal of Oral Science ›› 2019, Vol. 11 ›› Issue (3) : 26 DOI: 10.1038/s41368-019-0061-2
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Divide and conquer: two stem cell populations in squamous epithelia, reserves and the active duty forces

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Abstract

Stem cells are of great interest to the scientific community due to their potential role in regenerative and rejuvenative medicine. However, their role in the aging process and carcinogenesis remains unclear. Because DNA replication in stem cells may contribute to the background mutation rate and thereby to cancer, reducing proliferation and establishing a relatively quiescent stem cell compartment has been hypothesized to limit DNA replication-associated mutagenesis. On the other hand, as the main function of stem cells is to provide daughter cells to build and maintain tissues, the idea of a quiescent stem cell compartment appears counterintuitive. Intriguing observations in mice have led to the idea of separated stem cell compartments that consist of cells with different proliferative activity. Some epithelia of short-lived rodents appear to lack quiescent stem cells. Comparing stem cells of different species and different organs (comparative stem cell biology) may allow us to elucidate the evolutionary pressures such as the balance between cancer and longevity that govern stem cell biology (evolutionary stem cell biology). The oral mucosa and its stem cells are an exciting model system to explore the characteristics of quiescent stem cells that have eluded biologists for decades.

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Spencer Dunaway, Alexandra Rothaus, Yuhang Zhang, Ana Luisa Kadekaro, Thomas Andl, Claudia D. Andl. Divide and conquer: two stem cell populations in squamous epithelia, reserves and the active duty forces. International Journal of Oral Science, 2019, 11(3): 26 DOI:10.1038/s41368-019-0061-2

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References

[1]

Li L, Clevers H. Coexistence of quiescent and active adult stem cells in mammals. Science, 2010, 327: 542-545.

[2]

Nagy JD, Victor EM, Cropper JH. Why don’t all whales have cancer? A novel hypothesis resolving Peto’s paradox. Integr. Comp. Biol., 2007, 47: 317-328.

[3]

Aristotle. On Longevity and the Shortness of Life (ebooks@adelaide, Adelaide, 350 BC).

[4]

Rubner, M. Das Problem der Lebensdauer und seine Beziehungen zu Wachstum und Ernährung. (Max Rubner-Institut, Oldenbourg, 1908).

[5]

Speakman JR. Correlations between physiology and lifespan-two widely ignored problems with comparative studies. Aging Cell, 2005, 4: 167-175.

[6]

Peto Richard. Quantitative implications of the approximate irrelevance of mammalian body size and lifespan to lifelong cancer risk. Philosophical Transactions of the Royal Society B: Biological Sciences, 2015, 370(1673): 20150198.

[7]

Rangarajan A, Weinberg RA. Opinion: comparative biology of mouse versus human cells: modelling human cancer in mice. Nat. Rev. Cancer, 2003, 3: 952-959.

[8]

Ikeno Y, Bronson RT, Hubbard GB, Lee S, Bartke A. Delayed occurrence of fatal neoplastic diseases in ames dwarf mice: correlation to extended longevity. J. Gerontol. A Biol. Sci. Med Sci., 2003, 58: 291-296.

[9]

Sulak, M. et al. TP53 copy number expansion is associated with the evolution of increased body size and an enhanced DNA damage response in elephants. eLife 5, https://doi.org/10.7554/eLife.11994 (2016).

[10]

Abegglen LM, . Potential mechanisms for cancer resistance in elephants and comparative cellular response to DNA damage in humans. JAMA, 2015, 314: 1850-1860.

[11]

Caulin AF, Maley CC. Peto’s Paradox: evolution’s prescription for cancer prevention. Trends Ecol. Evol., 2011, 26: 175-182.

[12]

Seluanov A, Gladyshev VN, Vijg J, Gorbunova V. Mechanisms of cancer resistance in long-lived mammals. Nat. Rev. Cancer, 2018, 18: 433-441.

[13]

Jones KB, Klein OD. Oral epithelial stem cells in tissue maintenance and disease: the first steps in a long journey. Int J. Oral. Sci., 2013, 5: 121-129.

[14]

Tomasetti C, . Role of stem-cell divisions in cancer risk. Nature, 2017, 548: E13-E14.

[15]

Tomasetti C, Vogelstein B. Cancer etiology. Variation in cancer risk among tissues can be explained by the number of stem cell divisions. Science, 2015, 347: 78-81.

[16]

Caulin Aleah F., Graham Trevor A., Wang Li-San, Maley Carlo C.. Solutions to Peto's paradox revealed by mathematical modelling and cross-species cancer gene analysis. Philosophical Transactions of the Royal Society B: Biological Sciences, 2015, 370(1673): 20140222.

[17]

Zhu L, . Multi-organ mapping of cancer risk. Cell, 2016, 166: 1132-1146 e1137.

[18]

Kim MJ, Kim MH, Kim SA, Chang JS. Age-related deterioration of hematopoietic stem cells. Int J. Stem Cells, 2008, 1: 55-63.

[19]

Schellhas HF, Heath G. Cell renewal in the human cervix uteri; a radioautographic study DNA, RNA, and protein synthesis. Am. J. Obstet. Gynecol., 1969, 104: 617-632.

[20]

Averette HE, Weinstein GD, Frost P. Autoradiographic analysis of cell proliferation kinetics in human genital tissues. I. Normal cervix and vagina. Am. J. Obstet. Gynecol., 1970, 108: 8-17.

[21]

Andl CD, . Association of TGFbeta signaling with the maintenance of a quiescent stem cell niche in human oral mucosa. Histochem. Cell Biol., 2016, 146: 539-555.

[22]

Kotelnikov VM, . Proliferation of epithelia of noninvolved mucosa in patients with head and neck cancer. Head. Neck, 1996, 18: 522-528.

[23]

Penneys NS, Fulton JE Jr., Weinstein GD, Frost P. Location of proliferating cells in human epidermis. Arch. Dermatol., 1970, 101: 323-327.

[24]

Thuringer JM. Regeneration of stratified squamous epithelium. Anat. Rec., 1929, 28: 31-43.

[25]

Lavker RM, Sun TT. Heterogeneity in epidermal basal keratinocytes: morphological and functional correlations. Science, 1982, 215: 1239-1241.

[26]

Preisler HD, . Continued malignant cell proliferation in head and neck tumors during cytotoxic therapy. Clin. Cancer Res., 1996, 2: 1453-1460.

[27]

Pan Q, . Identification of lineage-uncommitted, long-lived, label-retaining cells in healthy human esophagus and stomach, and in metaplastic esophagus. Gastroenterology, 2013, 144: 761-770.

[28]

Bosch FX, . Expression of the histone H3 gene in benign, semi-malignant and malignant lesions of the head and neck: a reliable proliferation marker. Eur. J. Cancer, 1993, 29A: 1454-1461.

[29]

Rumman M, Dhawan J, Kassem M. Concise review: quiescence in adult stem cells: biological significance and relevance to tissue regeneration. Stem Cells, 2015, 33: 2903-2912.

[30]

Coller HA, Sang L, Roberts JM. A new description of cellular quiescence. PLoS Biol., 2006, 4

[31]

Kwon JS, . Controlling depth of cellular quiescence by an Rb-E2F network switch. Cell Rep., 2017, 20: 3223-3235.

[32]

Oki T, . A novel cell-cycle-indicator, mVenus-p27K-, identifies quiescent cells and visualizes G0-G1 transition. Sci. Rep., 2014, 4

[33]

Litovchick L, Florens LA, Swanson SK, Washburn MP, DeCaprio JA. DYRK1A protein kinase promotes quiescence and senescence through DREAM complex assembly. Genes Dev., 2011, 25: 801-813.

[34]

Rodgers JT, . mTORC1 controls the adaptive transition of quiescent stem cells from G0 to G(Alert). Nature, 2014, 510: 393-396.

[35]

Sun A, Bagella L, Tutton S, Romano G, Giordano A. From G0 to S phase: a view of the roles played by the retinoblastoma (Rb) family members in the Rb-E2F pathway. J. Cell. Biochem., 2007, 102: 1400-1404.

[36]

Rivard N, L’Allemain G, Bartek J, Pouyssegur J. Abrogation of p27Kip1 by cDNA antisense suppresses quiescence (G0 state) in fibroblasts. J. Biol. Chem., 1996, 271: 18337-18341.

[37]

Yang JS, Lavker RM, Sun TT. Upper human hair follicle contains a subpopulation of keratinocytes with superior in vitro proliferative potential. J. Invest. Dermatol., 1993, 101: 652-659.

[38]

Reiss M, Sartorelli AC. Regulation of growth and differentiation of human keratinocytes by type beta transforming growth factor and epidermal growth factor. Cancer Res., 1987, 47: 6705-6709.

[39]

Reiss M, Stash EB. High frequency of resistance of human squamous carcinoma cells to the anti-proliferative action of transforming growth factor beta. Cancer Commun., 1990, 2: 363-369.

[40]

Lin HY, Yang LT. Differential response of epithelial stem cell populations in hair follicles to TGF-beta signaling. Dev. Biol., 2013, 373: 394-406.

[41]

Missero C, Ramon y Cajal S, Dotto GP. Escape from transforming growth factor beta control and oncogene cooperation in skin tumor development. Proc. Natl Acad. Sci. USA, 1991, 88: 9613-9617.

[42]

Andl T, . Concerted loss of TGFbeta-mediated proliferation control and E-cadherin disrupts epithelial homeostasis and causes oral squamous cell carcinoma. Carcinogenesis, 2014, 35: 2602-2610.

[43]

Booth D, Haley JD, Bruskin AM, Potten CS. Transforming growth factor-B3 protects murine small intestinal crypt stem cells and animal survival after irradiation, possibly by reducing stem-cell cycling. Int. J. Cancer, 2000, 86: 53-59.

[44]

Saini N, . The impact of environmental and endogenous damage on somatic mutation load in human skin fibroblasts. PLoS Genet., 2016, 12

[45]

Abyzov A, . One thousand somatic SNVs per skin fibroblast cell set baseline of mosaic mutational load with patterns that suggest proliferative origin. Genome Res., 2017, 27: 512-523.

[46]

Martincorena I, . Tumor evolution. High burden and pervasive positive selection of somatic mutations in normal human skin. Science, 2015, 348: 880-886.

[47]

Blokzijl F, . Tissue-specific mutation accumulation in human adult stem cells during life. Nature, 2016, 538: 260-264.

[48]

Lynch MRate. molecular spectrum, and consequences of human mutation. Proc. Natl Acad. Sci. USA, 2010, 107: 961-968.

[49]

Fujimaki K, Yao G. Crack the state of silence: tune the depth of cellular quiescence for cancer therapy. Mol. Cell Oncol., 2018, 5

[50]

Failla G. The aging process and cancerogenesis. Ann. N. Y Acad. Sci., 1958, 71: 1124-1140.

[51]

Vijg J, Dong X, Milholland B, Zhang L. Genome instability: a conserved mechanism of ageing?. Essays Biochem., 2017, 61: 305-315.

[52]

Clevers H. Stem cells. What is an adult stem cell?. Science, 2015, 350: 1319-1320.

[53]

Kaiko GE, . The colonic crypt protects stem cells from microbiota-derived metabolites. Cell, 2016, 165: 1708-1720.

[54]

Moskalev AA, . The role of DNA damage and repair in aging through the prism of Koch-like criteria. Ageing Res. Rev., 2013, 12: 661-684.

[55]

Nijnik A, . DNA repair is limiting for haematopoietic stem cells during ageing. Nature, 2007, 447: 686-690.

[56]

Rossi DJ, . Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature, 2007, 447: 725-729.

[57]

Lavasani M, . Muscle-derived stem/progenitor cell dysfunction limits healthspan and lifespan in a murine progeria model. Nat. Commun., 2012, 3

[58]

Beerman I, Seita J, Inlay MA, Weissman IL, Rossi DJ. Quiescent hematopoietic stem cells accumulate DNA damage during aging that is repaired upon entry into cell cycle. Cell Stem Cell, 2014, 15: 37-50.

[59]

Biechonski S, Milyavsky M. Differences between human and rodent DNA-damage response in hematopoietic stem cells: at the crossroads of self-renewal, aging and leukemogenesis. Rev. Transl. Cancer Res., 2013, 2: 372-383.

[60]

Chen BR, . Quiescent fibroblasts are more active in mounting robust inflammatory responses than proliferative fibroblasts. PLoS ONE, 2012, 7

[61]

Piccoli C, . To breathe or not to breathe: the haematopoietic stem/progenitor cells dilemma. Br. J. Pharm., 2013, 169: 1652-1671.

[62]

Eliasson P, Jonsson JI. The hematopoietic stem cell niche: low in oxygen but a nice place to be. J. Cell Physiol., 2010, 222: 17-22.

[63]

Valcourt JR, . Staying alive: metabolic adaptations to quiescence. Cell Cycle, 2012, 11: 1680-1696.

[64]

Nicholson AM, . Barrett’s metaplasia glands are clonal, contain multiple stem cells and share a common squamous progenitor. Gut, 2012, 61: 1380-1389.

[65]

Kawakatsu K, Mori M. Histochemical evaluation of enzymatic activities in human squamous-cell cancer. Cancer Res., 1963, 23: 539-545.

[66]

Eminaga Okyaz, Fries Jochen, Neiß Susanne, Heitmann Michaela, Wötzel Fabian, Heidenreich Axel, Bruns Christiane, Alakus Hakan, Warnecke-Eberz Ute. The upregulation of hypoxia-related miRNA 210 in primary tumor of lymphogenic metastatic prostate cancer. Epigenomics, 2018, 10(10): 1347-1359.

[67]

Mori M, Mizushima T, Koizumi K. A comparative histochemical evaluation of various dehydrogenases in the oral squamous epithelium. Zeitschrift für Zellforschung und mikroskopische Anatomie Abt. Histochemie, 1962, 3: 111-121.

[68]

Macpherson AJ, . Mitochondrial gene expression in the human gastrointestinal tract. J. Cell Sci., 1992, 102(Pt 2): 307-314.

[69]

Geisenheimer J, Han SS. A quantitative electron microscopic study of desmosomes and hemidesmosomes in human crevicular epithelium. J. Periodontol., 1971, 42: 396-405.

[70]

Meyer M, Schroeder HE. A quantitative electron microscopic analysis of the keratinizing epithelium of noral human hard palate. Cell Tissue Res., 1975, 158: 177-203.

[71]

Lemons JM, . Quiescent fibroblasts exhibit high metabolic activity. PLoS Biol., 2010, 8

[72]

Ayatollahi M, Hesami Z, Jamshidzadeh A, Gramizadeh B. Antioxidant effects of bone marrow mesenchymal stem cell against carbon tetrachloride-induced oxidative damage in rat livers. Int. J. Organ Transpl. Med., 2014, 5: 166-173.

[73]

Li M, . Stem cell transplantation increases antioxidant effects in diabetic mice. Int J. Biol. Sci., 2012, 8: 1335-1344.

[74]

Garcia-Prat L, Sousa-Victor P, Munoz-Canoves P. Proteostatic and metabolic control of stemness. Cell Stem Cell, 2017, 20: 593-608.

[75]

Ke Z, . Translation fidelity coevolves with longevity. Aging Cell, 2017, 16: 988-993.

[76]

Lee JW, . Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature, 2006, 443: 50-55.

[77]

Azpurua J, . Naked mole-rat has increased translational fidelity compared with the mouse, as well as a unique 28S ribosomal RNA cleavage. Proc. Natl Acad. Sci. USA, 2013, 110: 17350-17355.

[78]

Tuorto F, . The tRNA methyltransferase Dnmt2 is required for accurate polypeptide synthesis during haematopoiesis. EMBO J., 2015, 34: 2350-2362.

[79]

Blanco S, . Stem cell function and stress response are controlled by protein synthesis. Nature, 2016, 534: 335-340.

[80]

Frye M, Watt FM. The RNA methyltransferase Misu (NSun2) mediates Myc-induced proliferation and is upregulated in tumors. Curr. Biol., 2006, 16: 971-981.

[81]

Blanco S, . The RNA-methyltransferase Misu (NSun2) poises epidermal stem cells to differentiate. PLoS Genet., 2011, 7

[82]

Uhlen M, . Proteomics. Tissue-based map of the human proteome. Science, 2015, 347: 1260419.

[83]

Berglund L, . A genecentric Human Protein Atlas for expression profiles based on antibodies. Mol. Cell Proteom., 2008, 7: 2019-2027.

[84]

Uhlen M, . Towards a knowledge-based Human Protein Atlas. Nat. Biotechnol., 2010, 28: 1248-1250.

[85]

Gingold H, . A dual program for translation regulation in cellular proliferation and differentiation. Cell, 2014, 158: 1281-1292.

[86]

Calderwood SK, Murshid A, Prince T. The shock of aging: molecular chaperones and the heat shock response in longevity and aging-a mini-review. Gerontology, 2009, 55: 550-558.

[87]

Fan GC. Role of heat shock proteins in stem cell behavior. Prog. Mol. Biol. Transl. Sci., 2012, 111: 305-322.

[88]

Gogler-Piglowska A, . Novel role for the testis-enriched HSPA2 protein in regulating epidermal keratinocyte differentiation. J. Cell Physiol., 2018, 233: 2629-2644.

[89]

Hansen M, . Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell, 2007, 6: 95-110.

[90]

Vellai T, . Genetics: influence of TOR kinase on lifespan in C. elegans. Nature, 2003, 426: 620.

[91]

Kapahi P, . Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr. Biol., 2004, 14: 885-890.

[92]

Castilho RM, Squarize CH, Chodosh LA, Williams BO, Gutkind JS. mTOR mediates Wnt-induced epidermal stem cell exhaustion and aging. Cell Stem Cell, 2009, 5: 279-289.

[93]

Iglesias-Bartolome R, . mTOR inhibition prevents epithelial stem cell senescence and protects from radiation-induced mucositis. Cell Stem Cell, 2012, 11: 401-414.

[94]

Sonis S, Andreotta PW, Lyng G. On the pathogenesis of mTOR inhibitor-associated stomatitis (mIAS)-studies using an organotypic model of the oral mucosa. Oral. Dis., 2017, 23: 347-352.

[95]

Chen C, . TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J. Exp. Med., 2008, 205: 2397-2408.

[96]

Feldmeyer L, Hofbauer GF, Boni T, French LE, Hafner J. Mammalian target of rapamycin (mTOR) inhibitors slow skin carcinogenesis, but impair wound healing. Br. J. Dermatol, 2012, 166: 422-424.

[97]

Zhu Z, . Prevention of irradiation-induced salivary hypofunction by rapamycin in swine parotid glands. Oncotarget, 2016, 7: 20271-20281.

[98]

Ryan Weston Kenneth, Fernandez Josiah, Peterson Mikayla Katherine, Sheneman David William, Podell Brendan Keefe, De Subhajyoti, Torchia Enrique Carlo. Activation of S6 signaling is associated with cell survival and multinucleation in hyperplastic skin after epidermal loss of AURORA-A Kinase. Cell Death & Differentiation, 2018, 26(3): 548-564.

[99]

Buerger C, . Inflammation dependent mTORC1 signaling interferes with the switch from keratinocyte proliferation to differentiation. PLoS ONE, 2017, 12

[100]

Ding X, . mTORC1 and mTORC2 regulate skin morphogenesis and epidermal barrier formation. Nat. Commun., 2016, 7

[101]

Martins F, de Sousa SC, Dos Santos E, Woo SB, Gallottini M. PI3K-AKT-mTOR pathway proteins are differently expressed in oral carcinogenesis. J. Oral. Pathol. Med., 2016, 45: 746-752.

[102]

Clark C, . Teasing out the best molecular marker in the AKT/mTOR pathway in head and neck squamous cell cancer patients. Laryngoscope, 2010, 120: 1159-1165.

[103]

Amornphimoltham P, . Mammalian target of rapamycin, a molecular target in squamous cell carcinomas of the head and neck. Cancer Res., 2005, 65: 9953-9961.

[104]

Meng Delong, Frank Anderson R., Jewell Jenna L.. mTOR signaling in stem and progenitor cells. Development, 2018, 145(1): dev152595.

[105]

Deng Z, . mTOR signaling promotes stem cell activation via counterbalancing BMP-mediated suppression during hair regeneration. J. Mol. Cell Biol., 2015, 7: 62-72.

[106]

Liu NB, . High DEPTOR expression correlates with poor prognosis in patients with esophageal squamous cell carcinoma. Onco Targets Ther., 2015, 8: 3449-3455.

[107]

Rabanal-Ruiz Y, Otten EG, Korolchuk VI. mTORC1 as the main gateway to autophagy. Essays Biochem., 2017, 61: 565-584.

[108]

El-Houjeiri Leeanna, Possik Elite, Vijayaraghavan Tarika, Paquette Mathieu, Martina José A., Kazan Jalal M., Ma Eric H., Jones Russell, Blanchette Paola, Puertollano Rosa, Pause Arnim. The Transcription Factors TFEB and TFE3 Link the FLCN-AMPK Signaling Axis to Innate Immune Response and Pathogen Resistance. Cell Reports, 2019, 26(13): 3613-3628.e6.

[109]

Yang M, . Emerging roles and regulation of MiT/TFE transcriptional factors. Cell Commun. Signal, 2018, 16

[110]

Lipina C, Hundal HS. Is REDD1 a metabolic eminence grise?. Trends Endocrinol. Metab., 2016, 27: 868-880.

[111]

Bernardi R, . Pml represses tumour progression through inhibition of mTOR. EMBO Mol. Med., 2011, 3: 249-257.

[112]

Wouters BG, Koritzinsky M. Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat. Rev. Cancer, 2008, 8: 851-864.

[113]

Hsu KS, Kao HY. PML: regulation and multifaceted function beyond tumor suppression. Cell Biosci., 2018, 8: 5.

[114]

Cheng X, Kao HY. Post-translational modifications of PML: consequences and implications. Front. Oncol., 2012, 2: 210.

[115]

Grimm M, . Association of cancer metabolism-related proteins with oral carcinogenesis - indications for chemoprevention and metabolic sensitizing of oral squamous cell carcinoma?. J. Transl. Med, 2014, 12

[116]

Reichenbach, B. et al. Glutamate transporter Slc1a3 mediates inter-niche stem cell activation during skin growth. EMBO J. 37, https://doi.org/10.15252/embj.201798280 (2018).

[117]

Day TA, . Inhibition of mTOR signaling and clinical activity of rapamycin in head and neck cancer in a window of opportunity trial. Clin. Cancer Res., 2019, 25: 1156-1164.

[118]

Guan JL, . Autophagy in stem cells. Autophagy, 2013, 9: 830-849.

[119]

Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell, 2011, 147: 728-741.

[120]

Ho TT, . Autophagy maintains the metabolism and function of young and old stem cells. Nature, 2017, 543: 205-210.

[121]

Vilchez D, Simic MS, Dillin A. Proteostasis and aging of stem cells. Trends Cell Biol., 2014, 24: 161-170.

[122]

Rodolfo C, Di Bartolomeo S, Cecconi F. Autophagy in stem and progenitor cells. Cell Mol. Life Sci., 2016, 73: 475-496.

[123]

Sigurdsson V, Miharada K. Regulation of unfolded protein response in hematopoietic stem cells. Int J. Hematol., 2018, 107: 627-633.

[124]

Yang Y, Cheung HH, Tu J, Miu KK, Chan WY. New insights into the unfolded protein response in stem cells. Oncotarget, 2016, 7: 54010-54027.

[125]

Ermolaeva M, Neri F, Ori A, Rudolph KL. Cellular and epigenetic drivers of stem cell ageing. Nat. Rev. Mol. Cell Biol., 2018, 19: 594-610.

[126]

Hayflick L. How and why we age. Exp. Gerontol., 1998, 33: 639-653.

[127]

Hayflick L. “Anti-aging” is an oxymoron. J. Gerontol. A Biol. Sci. Med Sci., 2004, 59: B573-B578.

[128]

Yan KS, . The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations. Proc. Natl Acad. Sci. USA, 2012, 109: 466-471.

[129]

Park IK, . Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature, 2003, 423: 302-305.

[130]

Jones M, . Ash1l controls quiescence and self-renewal potential in hematopoietic stem cells. J. Clin. Investig., 2015, 125: 2007-2020.

[131]

Frangini A, . The aurora B kinase and the polycomb protein ring1B combine to regulate active promoters in quiescent lymphocytes. Mol. Cell, 2013, 51: 647-661.

[132]

Shima H, . Ring1A and Ring1B inhibit expression of Glis2 to maintain murine MOZ-TIF2 AML stem cells. Blood, 2018, 131: 1833-1845.

[133]

Boukhaled GM, . The transcriptional repressor polycomb group factor 6, PCGF6, negatively regulates dendritic cell activation and promotes quiescence. Cell Rep., 2016, 16: 1829-1837.

[134]

Jones KB, . Quantitative clonal analysis and single-cell transcriptomics reveal division kinetics, hierarchy, and fate of oral epithelial progenitor cells. Cell Stem Cell, 2019, 24: 183-192.e188.

[135]

Owen RP, . Single cell RNA-seq reveals profound transcriptional similarity between Barrett’s oesophagus and oesophageal submucosal glands. Nat. Commun., 2018, 9

[136]

Matthias C, Mack B, Berghaus A, Gires O. Keratin 8 expression in head and neck epithelia. BMC Cancer, 2008, 8

[137]

Machado L, . In situ fixation redefines quiescence and early activation of skeletal muscle stem cells. Cell Rep., 2017, 21: 1982-1993.

[138]

van den Brink SC, . Single-cell sequencing reveals dissociation-induced gene expression in tissue subpopulations. Nat. Methods, 2017, 14: 935-936.

[139]

Potten CS, Loeffler M. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons Crypt. Dev., 1990, 110: 1001-1020.

[140]

Kennedy-Crispin M, . Human keratinocytes’ response to injury upregulates CCL20 and other genes linking innate and adaptive immunity. J. Invest. Dermatol., 2012, 132: 105-113.

[141]

Luan L, Shi J, Yu Z, Andl T. The major miR-31 target genes STK40 and LATS2 and their implications in the regulation of keratinocyte growth and hair differentiation. Exp. Dermatol., 2017, 26: 497-504.

[142]

Agarwal, V., Bell, G. W., Nam, J. W. & Bartel, D. P. Predicting effective microRNA target sites in mammalian mRNAs. eLife 4, https://doi.org/10.7554/eLife.05005 (2015).

[143]

Ning MS, Andl T. Concise review: custodians of the transcriptome: how microRNAs guard stemness in squamous epithelia. Stem Cells, 2015, 33: 1047-1054.

[144]

Rhee WJ, Bao G. Simultaneous detection of mRNA and protein stem cell markers in live cells. BMC Biotechnol., 2009, 9

[145]

Subramaniam S, . Distinct transcriptional networks in quiescent myoblasts: a role for Wnt signaling in reversible vs. irreversible arrest. PLoS ONE, 2014, 8

[146]

Shapiro HM. Flow cytometric estimation of DNA and RNA content in intact cells stained with Hoechst 33342 and pyronin Y. Cytometry, 1981, 2: 143-150.

[147]

Kim KH, Sederstrom JM. Assaying cell cycle status using flow cytometry. Curr. Protoc. Mol. Biol., 2015, 111: 28.6.1-28.6.11.

[148]

Aida J, . Basal cells have longest telomeres measured by tissue Q-FISH method in lingual epithelium. Exp. Gerontol., 2008, 43: 833-839.

[149]

Aida J, . Short telomeres in an oral precancerous lesion: Q-FISH analysis of leukoplakia. J. Oral. Pathol. Med, 2012, 41: 372-378.

[150]

Takubo K, . Q-FISH analysis of telomere and chromosome instability in the oesophagus with and without squamous cell carcinoma in situ. J. Pathol., 2010, 221: 201-209.

[151]

Fujimoto R, . Expression of telomerase components in oral keratinocytes and squamous cell carcinomas. Oral. Oncol., 2001, 37: 132-140.

[152]

Kammori M, . Squamous cell carcinomas of the esophagus arise from a telomere-shortened epithelial field. Int J. Mol. Med., 2007, 20: 793-799.

[153]

Aida J, . Telomere lengths in the oral epithelia with and without carcinoma. Eur. J. Cancer, 2010, 46: 430-438.

[154]

Sunpaweravong S, Sunpaweravong P, Sathitruangsak C, Mai S. Three-dimensional telomere architecture of esophageal squamous cell carcinoma: comparison of tumor and normal epithelial cells. Dis. Esophagus, 2016, 29: 307-313.

[155]

Qin HD, . Genomic characterization of esophageal squamous cell carcinoma reveals critical genes underlying tumorigenesis and poor prognosis. Am. J. Hum. Genet., 2016, 98: 709-727.

[156]

Tan DW, . Single-cell gene expression profiling reveals functional heterogeneity of undifferentiated human epidermal cells. Development, 2013, 140: 1433-1444.

[157]

Jensen KB, Watt FM. Single-cell expression profiling of human epidermal stem and transit-amplifying cells: Lrig1 is a regulator of stem cell quiescence. Proc. Natl Acad. Sci. USA, 2006, 103: 11958-11963.

[158]

Schluter H, Paquet-Fifield S, Gangatirkar P, Li J, Kaur P. Functional characterization of quiescent keratinocyte stem cells and their progeny reveals a hierarchical organization in human skin epidermis. Stem Cells, 2011, 29: 1256-1268.

[159]

Kocer SS, Djuric PM, Bugallo MF, Simon SR, Matic M. Transcriptional profiling of putative human epithelial stem cells. BMC Genome, 2008, 9

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