New insights into the role of Runx1 in epithelial stem cell biology and pathology

Journal of Cellular Biochemistry

Volumn 114, Issue 5, 2013, Pages 985-993

  Scheitz, Cornelia Johanna Franziska ^a   Tumbar, Tudorita ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

breast cancer; endometroid carcinoma; hair follicle stem cells; intestinal cancer; oral epithelium stem cells; Runx1; squamous cell carcinoma

Indexed keywords

RAS PROTEIN; TRANSCRIPTION FACTOR RUNX1;

ARTICLE; AUTOIMMUNE DISEASE; CANCER CELL; CARCINOGENESIS; CYTOLOGY; DERMIS; EPITHELIUM CELL; HAIR FOLLICLE; HUMAN; MOUTH MUCOSA; NONHUMAN; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; SKIN CANCER; SKIN TUMOR; SOLID TUMOR; STEM CELL;

ANIMALS; AUTOIMMUNE DISEASES; CORE BINDING FACTOR ALPHA 2 SUBUNIT; EPITHELIAL CELLS; HAIR FOLLICLE; HUMANS; NEOPLASMS; STEM CELLS;

EID: 84875157758     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24453     Document Type: Article

References (51)

1. Alam M, Ratner D,. 2001. Cutaneous squamous cell carcinoma. N Engl J Med 344: 975-983.
2. Banerji S, Cibulskis K, Rangel-Escareno C, Brown KK, Carter SL, Frederick AM, Lawrence MS, Sivachenko AY, Sougnez C, Zou L, Cortes ML, Fernandez-Lopez JC, Peng S, Ardlie KG, Auclair D, Bautista-Piña V, Duke F, Francis J, Jung J, Maffuz-Aziz A, Onofrio RC, Parkin M, Pho NH, Quintanar-Jurado V, Ramos AH, Rebollar-Vega R, Rodriguez-Cuevas S, Romero-Cordoba SL, Schumacher SE, Stransky N, Thompson KM, Uribe-Figueroa L, Baselga J, Beroukhim R, Polyak K, Sgroi DC, Richardson AL, Jimenez-Sanchez G, Lander ES, Gabriel SB, Garraway La, Golub TR, Melendez-Zajgla J, Toker A, Getz G, Hidalgo-Miranda A, Meyerson M,. 2012. Sequence analysis of mutations and translocations across breast cancer subtypes. Nature 486: 405-409.
3. Barker N, Ridgway Ra, van Es JH, van de Wetering M, Begthel H, van den Born M, Danenberg E, Clarke AR, Sansom OJ, Clevers H,. 2009. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457: 608-611.
4. Challen GA, Goodell MA,. 2010. Runx1 isoforms show differential expression patterns during hematopoietic development but have similar functional effects in adult hematopoietic stem cells. Exp Hematol 38: 403-416.
5. Chen MJ, Yokomizo T, Zeigler BM, Dzierzak E, Speck NA,. 2009. Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457: 887-891.
6. Fife BT, Pauken KE,. 2011. The role of the PD-1 pathway in autoimmunity and peripheral tolerance. Ann N Y Acad Sci 1217: 45-59.
7. Fijneman RJA, Anderson RA, Richards E, Liu J, Tijssen M, Meijer GA, Anderson J, Rod A, O'Sullivan MG, Scott PM, Cormier RT,. 2012. Runx1 is a tumor suppressor gene in the mouse gastrointestinal tract. Cancer Sci 103: 593-599.
8. Friedman AD,. 2009. Cell cycle and developmental control of hematopoiesis by Runx1. J Cell Physiol 219: 520-524.
9. Ghozi MC, Bernstein Y, Negreanu V, Levanon D, Groner Y,. 1996. Expression of the human acute myeloid leukemia gene AML1 is regulated by two promoter regions. Proc Natl Acad Sci USA 93: 1935-1940.
10. Griffi CEM, Barker JNWN,. 2007. Psoriasis 1 pathogenesis and clinical features of psoriasis. Lancet 370: 264-271.
11. Helms C, Cao L, Krueger JG, Wijsman EM, Chamian F, Gordon D, Heffernan M, Daw JAW, Robarge J, Ott J, Kwok P-Y, Menter A, Bowcock AM,. 2003. A putative Runx1 binding site variant between SLC9A3R1 and NAT9 is associated with susceptibility to psoriasis. Nat Genet 35: 349-356.
12. Hoi C, Lee SE, Lu S-Y, McDermitt DJ, Osorio KM, Piskun C, Peters R, Paus R, Tumbar T,. 2010. Runx1 directly promotes proliferation of hair follicle stem cells and epithelial tumor formation in mouse skin. Mol Cell Biol 30: 2518-2536.
13. Huang S-P, Lan Y-H, Lu T-L, Pao J-B, Chang T-Y, Lee H-Z, Yang W-H, Hsieh C-J, Chen L-M, Huang L-C, Ting W-C, Bao B-Y,. 2011. Clinical significance of runt-related transcription factor 1 polymorphism in prostate cancer. BJU Int 107: 486-492.
14. Ishimatsu-Tsuji Y, Moro O, Kishimoto J,. 2005. Expression profiling and cellular localization of genes associated with the hair cycle induced by wax depilation. J Invest Dermatol 125: 410-420.
15. Kanaykina N, Abelson K, King D, Liakhovitskaia A, Schreiner S, Wegner M, Kozlova EN,. 2010. In vitro and in vivo effects on neural crest stem cell differentiation by conditional activation of Runx1 short isoform and its effect on neuropathic pain behavior. Ups J Med Sci 115: 56-64.
16. Kurokawa M, Tanaka T, Tanaka K, Hirano N, Ogawa S, Mitani K, Yazaki Y, Hirai H,. 1996. A conserved cysteine residue in the runt homology domain of AML1 is required for the DNA binding ability and the transforming activity on fibroblasts. J Biol Chem 271: 16870-16876.
17. Lapouge G, Youssef KK, Vokaer B, Achouri Y, Michaux C, Sotiropoulou Pa, Blanpain C,. 2011. Identifying the cellular origin of squamous skin tumors. Proc Natl Acad Sci USA 108: 7431-7436.
18. Lee J, Tumbar T,. 2012. Hairy tale of signaling in hair follicle development and cycling. Semin Cell Dev Biol 23: 906-916.
19. Levanon D, Brenner O, Negreanu V, Bettoun D, Woolf E, Eilam R, Lotem J, Gat U, Otto F, Speck N, Groner Y,. 2001. Spatial and temporal expression pattern of Runx3 (Aml2) and Runx1 (Aml1) indicates non-redundant functions during mouse embryogenesis. Mech Dev 109: 413-417.
20. Mangan JK, Speck NA,. 2011. Runx1 mutations in clonal myeloid disorders: From conventional cytogenetics to next generation sequencing, a story 40 years in the making. Crit Rev Oncog 16: 77-91.
21. Merrill B, Gat U, DasGupta R, Fuchs E,. 2001. Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes Dev 15: 1688-1705.
22. Miyoshi H, Shimizu K, Kozu T, Maseki N, Kaneko Y, Ohki M,. 1991. t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia are clustered within a limited region of a single gene, AML1. Proc Natl Acad Sci USA 88: 10431-10434.
23. Monge M, Colas E, Doll A, Gonzalez M, Gil-Moreno A, Planaguma J, Quiles M, Arbos MA, Garcia A, Castellvi J, Llaurado M, Rigau M, Alazzouzi H, Xercavins J, Alameda F, Reventos J, Abal M,. 2007. ERM/ETV5 up-regulation plays a role during myometrial infiltration through matrix metalloproteinase-2 activation in endometrial cancer. Cancer Res 67: 6753-6759.
24. Morris RJ, Liu Y, Marles L, Yang Z, Trempus C, Li S, Lin JS, Sawicki Ja, Cotsarelis G,. 2004. Capturing and profiling adult hair follicle stem cells. Nat Biotechnol 22: 411-417.
25. Ortt K, Raveh E, Gat U, Sinha S,. 2008. A chromatin immunoprecipitation screen in mouse keratinocytes reveals Runx1 as a direct transcriptional target of DNp63. J Cell Biochem 1219: 1204-1219.
26. Osorio KM, Lee SE, McDermitt DJ, Waghmare SK, Zhang YV, Woo HN, Tumbar T,. 2008. Runx1 modulates developmental, but not injury-driven, hair follicle stem cell activation. Development (Cambridge, England) 135: 1059-1068.
27. Osorio KM, Lilja KC, Tumbar T,. 2011. Runx1 modulates adult hair follicle stem cell emergence and maintenance from distinct embryonic skin compartments. J Cell Biol 193: 235-250.
28. Planagumà J, Díaz-Fuertes M, Gil-Moreno A, Abal M, Monge M, García A, Barõ T, Thomson TM, Xercavins J, Alameda F, Reventõs J,. 2004. A differential gene expression profile reveals overexpression of Runx1/AML1 in invasive endometrioid carcinoma. Cancer Res 64: 8846-8853.
29. Planagumà J, Gonzalez M, Doll A, Monge M, Gil-Moreno A, Barõ T, García A, Xercavins J, Alameda F, Abal M, Reventõs J,. 2006. The up-regulation profiles of p21WAF1/CIP1 and Runx1/AML1 correlate with myometrial infiltration in endometrioid endometrial carcinoma. Hum Pathol 37: 1050-1057.
30. Planagumà J, Liljeström M, Alameda F, Bützow R, Virtanen I, Reventõs J, Hukkanen M,. 2011. Matrix metalloproteinase-2 and matrix metalloproteinase-9 codistribute with transcription factors Runx1/AML1 and ETV5/ERM at the invasive front of endometrial and ovarian carcinoma. Hum Pathol 42: 57-67.
31. Polakis P,. 2012. Wnt signaling in cancer. Cold Spring Harb Perspect Biol 4: a008052.
32. Pradhan MP, Prasad NK, Palakal MJ,. 2012. A systems biology approach to the global analysis of transcription factors in colorectal cancer. BMC Cancer 12: 331.
33. Pratap J, Javed A, Languino LR, Andre J, Wijnen V, Stein JL, Stein GS, Lian JB,. 2005. The Runx2 osteogenic transcription factor regulates matrix metalloproteinase 9 in bone metastatic cancer cells and controls cell invasion. Mol Cell Biol 25: 8581-8591.
34. Prokunina L, Castillejo-Lõpez C, Oberg F, Gunnarsson I, Berg L, Magnusson V, Brookes AJ, Tentler D, Kristjansdõttir H, Gröndal G, Bolstad AI, Svenungsson E, Lundberg I, Sturfelt G, Jönssen A, Truedsson L, Lima G, Alcocer-Varela J, Jonsson R, Gyllensten UB, Harley JB, Alarcõn-Segovia D, Steinsson K, Alarcõn-Riquelme ME,. 2002. A regulatory polymorphism in PDCD1 is associated with susceptibility to systemic lupus erythematosus in humans. Nat Genet 32: 666-669.
35. Raveh E, Cohen S, Levanon D, Negreanu V, Groner Y, Gat U,. 2006. Dynamic expression of Runx1 in skin affects hair structure. Mech Dev 123: 842-850.
36. Sano S, Itami S, Takeda K, Tarutani M, Yamaguchi Y, Miura H, Yoshikawa K, Akira S, Takeda J,. 1999. Keratinocyte-specific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis. EMBO J 18: 4657-4668.
37. Sano S, Kira M, Takagi S, Yoshikawa K, Takeda J, Itami S,. 2000. Two distinct signaling pathways in hair cycle induction: Stat3-dependent and -independent pathways. Proc Natl Acad Sci USA 97: 13824-13829.
38. Scheitz CJF, Lee TS, McDermitt D, Tumbar T,. 2012. Defining a tissue stem cell-driven Runx1/Stat3 signalling axis in epithelial cancer. EMBO 31: 4124-4139.
39. Schneider MR, Schmidt-Ullrich R, Paus R,. 2009. The hair follicle as a dynamic miniorgan. Curr Biol 19: R132-R142.
40. Slattery ML, Lundgreen A, Herrick JS, Caan BJ, Potter JD, Wolff RK,. 2011. Associations between genetic variation in Runx1, Runx2, Runx3, MAPK1 and eIF4E and risk of colon and rectal cancer: Additional support for a TGF-β-signaling pathway. Carcinogenesis 32: 318-326.
41. Soma T, Ishimatsu-Tsuji Y, Tajima M, Kishimoto J,. 2006. Runx1 transcription factor is involved in the regulation of KAP5 gene expression in human hair follicles. J Dermatol Sci 41: 221-224.
42. Tokuhiro S, Yamada R, Chang X, Suzuki A, Kochi Y, Sawada T, Suzuki M, Nagasaki M, Ohtsuki M, Ono M, Furukawa H, Nagashima M, Yoshino S, Mabuchi A, Sekine A, Saito S, Takahashi A, Tsunoda T, Nakamura Y, Yamamoto K,. 2003. An intronic SNP in a Runx1 binding site of SLC22A4, encoding an organic cation transporter, is associated with rheumatoid arthritis. Nat Genet 35: 341-348.
43. Tumbar T, Guasch G, Greco V, Blanpain C, Lowry WE, Rendl M, Fuchs E,. 2004. Defining the epithelial stem cell niche in skin. Science (New York, NY) 303: 359-363.
44. Waghmare SK, Bansal R, Lee J, Zhang YV, McDermitt DJ, Tumbar T,. 2008. Quantitative proliferation dynamics and random chromosome segregation of hair follicle stem cells. EMBO J 27: 1309-1320.
45. Wang L, Brugge JS, Janes KA,. 2011. Intersection of FOXO- and Runx1-mediated gene expression programs in single breast epithelial cells during morphogenesis and tumor progression. Proc Natl Acad Sci 108: E803-E812.
46. White AC, Tran K, Khuu J, Dang C, Cui Y, Binder SW, Lowry WE,. 2011. Defining the origins of Ras/p53-mediated squamous cell carcinoma. Proc Natl Acad Sci USA 108: 7425-7430.
47. Yan J, Liu Y, Lukasik SM, Speck NA, Bushweller JH,. 2004. CBFbeta allosterically regulates the Runx1 Runt domain via a dynamic conformational equilibrium. Nat Struct Mol Biol 11: 901-906.
48. Yeh H-Y, Cheng S-W, Lin Y-C, Yeh C-Y, Lin S-F, Soo V-W,. 2009. Identifying significant genetic regulatory networks in the prostate cancer from microarray data based on transcription factor analysis and conditional independency. BMC Med Genomics 2: 70.
49. Yoshimi M, Goyama S, Kawazu M, Nakagawa M, Ichikawa M, Imai Y, Kumano K, Asai T, Mulloy JC, Kraft AS, Takahashi T, Shirafuji N, Kurokawa M,. 2012. Multiple phosphorylation sites are important for Runx1 activity in early hematopoiesis and T-cell differentiation. Eur J Immunol 42: 1044-1050.
50. Yuen H-F, McCrudden CM, Chan K-K, Chan Y-P, Wong ML-Y, Chan KY-K, Khoo U-S, Law S, Srivastava G, Lappin TR, Chan K-W, El-Tanani M,. 2011. The role of Pea3 group transcription factors in esophageal squamous cell carcinoma. Am J Pathol 179: 992-1003.
51. Zhang YV, Cheong J, Ciapurin N, McDermitt DJ, Tumbar T,. 2009. Distinct self-renewal and differentiation phases in the niche of infrequently dividing hair follicle stem cells. Cell Stem Cell 5: 267-278.