Multiclonal tumor origin: Evidence and implications

Parsons, 2008, Many different tumor types have polyclonal tumor origin: evidence and implications, Mutat. Res. - Rev. Mutat. Res., 659, 232, 10.1016/j.mrrev.2008.05.004

NIH, 1999

Diaz, 2012, The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers, Nature, 486, 537, 10.1038/nature11219

Parsons, 2013, KRAS mutant tumor subpopulations can subvert durable responses to personalized cancer treatments, Pers. Med., 10, 191, 10.2217/pme.13.1

Wang, 2011, Cancer stem cells, 128

Dhingra, 2013, Cancer stem cells

Nowell, 1976, The clonal evolution of tumor cell populations, Science, 194, 23, 10.1126/science.959840

Hahn, 2015, Cancer: a genetic disorder

Weinberg, 2014, The nature of cancer

Garcia, 1999, Field cancerization, clonality, and epithelial stem cells: the spread of mutated clones in epithelial sheets, J. Pathol., 187, 61, 10.1002/(SICI)1096-9896(199901)187:1<61::AID-PATH247>3.0.CO;2-I

Black, 2016, Cancer biology and genetics

NCI, 2015

Attolini, 2010, A mathematical framework to determine the temporal sequence of somatic genetic events in cancer, Proc. Natl. Acad. Sci. U. S. A., 107, 17604, 10.1073/pnas.1009117107

Parsons, 2011, Monoclonal tumor origin is an underlying misconception of the RESIC approach, Proc. Natl. Acad. Sci. U. S. A., 108, E15, 10.1073/pnas.1017998108

Cheng, 2011, Reply to Parsons: many tumor types follow the monoclonal model of tumor initiation, Proc. Natl. Acad. Sci. U. S. A., 108, E16, 10.1073/pnas.1018584108

Ramazzotti, 2017, Learning mutational graphs of individual tumor evolution from multi-sample sequencing data, bioRxiv

Cheng, 2013, Laser-assisted microdissection in translational research: theory, technical considerations, and future applications, Appl. Immunohistochem. Mol. Morphol., 21, 31, 10.1097/PAI.0b013e31824d0519

Agarwal, 2009, Does HUMARA assay for assessment of clonal hematopoiesis have shortcomings?, Blood, 114, 2357, 10.1182/blood-2009-04-217653

Chen, 2007, X-Linked clonality testing: interpretation and limitations, Blood, 110, 1411, 10.1182/blood-2006-09-018655

Jones, 2014, Nonrandom x chromosome inactivation detection

Hellman, 2007, Gene body-specific methylation on the active X chromosome, Science, 315, 1141, 10.1126/science.1136352

Carrel, 2005, X-Inactivation profile reveals extensive variability in X-linked gene expression in females, Nature, 434, 400, 10.1038/nature03479

Chaligné, 2014, X-Chromosome inactivation in development and cancer, FEBS Lett., 588, 2514, 10.1016/j.febslet.2014.06.023

Leedham, 2008, Human tumour clonality assessment–flawed but necessary, J. Pathol., 215, 351, 10.1002/path.2379

Wang, 2014, X-Chromosome genetic association test accounting for X-inactivation, skewed X-inactivation, and escape from X-inactivation, Genet. Epidemiol., 38, 483, 10.1002/gepi.21814

Mossner, 2010, Blood, 116, 977, 10.1182/blood.V116.21.977.977

Knudsen, 2007, Increased skewing of X chromosome inactivation with age in both blood and buccal cells, Cytogenet. Genome Res., 116, 24, 10.1159/000097414

Swierczek, 2008, Hematopoiesis is not clonal in healthy elderly women, Blood, 112, 3186, 10.1182/blood-2008-03-143925

Novelli, 2003, X-inactivation patch size in human female tissue confounds the assessment of tumor clonality, Proc. Natl. Acad. Sci. U. S. A., 100, 3311, 10.1073/pnas.0437825100

Merritt, 1997, Polyclonal structure of intestinal adenomas in Apc+ min/+ mice with concomitant loss of Apc++ from all tumor lineages, Proc. Natl. Acad. Sci. U. S. A., 94, 13927, 10.1073/pnas.94.25.13927

Thliveris, 2005, Polyclonality of familial murine adenomas: analyses of mouse chimeras with low tumor multiplicity suggest short-range interactions, Proc. Natl. Acad. Sci. U. S. A., 102, 6960, 10.1073/pnas.0502662102

Novelli, 1996, Polyclonal origin of colonic adenomas in an XO/XY patient with FAP, Science, 272, 1187, 10.1126/science.272.5265.1187

Jovanovic, 2003, Thyroid gland clonality revisited: the embryonal patch size of the normal human thyroid gland is very large, suggesting X-chromosome inactivation tumor clonality studies of thyroid tumors have to be interpreted with caution, J. Clin. Endocrinol. Metab., 88, 3284, 10.1210/jc.2002-021552

Moore, 1991, Cell growth simulations predicting polyclonal origins for’ monoclonal’ tumors, Cancer Lett., 60, 113, 10.1016/0304-3835(91)90217-6

Pozo-Garcia, 2003, Clonal origin and expansions in neoplasms: biologic and technical aspects must be considered together [1] (multiple letters), Am. J. Pathol., 162, 353, 10.1016/S0002-9440(10)63826-6

Levy, 2001, Monoclonality of endocrine tumours: what does it mean?, Trends Endocrinol. Metab., 12, 301, 10.1016/S1043-2760(01)00434-9

Swierczek, 2015, Presence of polyclonal hematopoiesis in females with Ph-negative myeloproliferative neoplasms, Leukemia, 29, 2432, 10.1038/leu.2015.249

Musalkova, 2015, Identification of novel informative loci for DNA-based X-inactivation analysis, Blood Cells Mol. Dis., 54, 210, 10.1016/j.bcmd.2014.10.001

Tukiainen, 2017, Landscape of X chromosome inactivation across human tissues, Nature, 550, 244, 10.1038/nature24265

Niho, 1999, Monoclonality of atypical adenomatous hyperplasia of the lung, Am. J. Pathol., 154, 249, 10.1016/S0002-9440(10)65271-6

Li, 2007, Clonality analysis of intraductal proliferative lesions using the human androgen receptor assay, Neoplasma, 54, 490

Gong, 2014, Dysplastic nodules with glypican-3 positive immunostaining: a risk for early hepatocellular carcinoma, PLoS One, 9, e87120, 10.1371/journal.pone.0087120

Ueda, 2008, Clonality and HPV infection analysis of concurrent glandular and squamous lesions and adenosquamous carcinomas of the uterine cervix, Am. J. Clin. Pathol., 130, 389, 10.1309/ERR93AF840YYNDRQ

Zheng, 2010, Clonality and TP53 mutation analysis of focal nodular hyperplasia of the liver, Am. J. Clin. Pathol., 134, 65, 10.1309/AJCPCIAH79EABQKM

Yu, 2009, Analysis of the progression of intraductal proliferative lesions in the breast by PCR-based clonal assay, Breast Cancer Res. Treat., 114, 433, 10.1007/s10549-008-0029-y

Gong, 2009, Use of X-chromosome inactivation pattern and laser microdissection to determine the clonal origin of focal nodular hyperplasia of the liver, Pathology, 41, 348, 10.1080/00313020902885029

Baker, 2013, Pre-tumour clones, periodic selection and clonal interference in the origin and progression of gastrointestinal cancer: potential for biomarker development, J. Pathol., 229, 502, 10.1002/path.4157

Teixeira, 2011, Cytogenetic Analysis of Tumor Clonality, Adv. Cancer Res., 127, 10.1016/B978-0-12-387688-1.00005-3

Salk, 2010, Passenger mutations as a marker of clonal cell lineages in emerging neoplasia, Semin. Cancer Biol., 20, 294, 10.1016/j.semcancer.2010.10.008

Brash, 2016, How do mutant clones expand in normal tissue?

Navin, 2015, The first five years of single-cell cancer genomics and beyond, Genome Res., 25, 1499, 10.1101/gr.191098.115

Davis, 2016, Computing tumor trees from single cells, Genome Biol., 17, 113, 10.1186/s13059-016-0987-z

Janiszewska, 2015, In situ single-cell analysis identifies heterogeneity for PIK3CA mutation and HER2 amplification in HER2-positive breast cancer, Nat. Genet., 47, 1212, 10.1038/ng.3391

Potter, 2013, Single-cell mutational profiling and clonal phylogeny in cancer, Genome Res., 23, 2115, 10.1101/gr.159913.113

Wang, 2014, Clonal evolution in breast cancer revealed by single nucleus genome sequencing, Nature, 512, 155, 10.1038/nature13600

Yu, 2014, Discovery of biclonal origin and a novel oncogene SLC12A5 in colon cancer by single-cell sequencing, Cell Res., 24, 701, 10.1038/cr.2014.43

Francis, 2014, EGFR variant heterogeneity in glioblastoma resolved through single-nucleus sequencing, Cancer Discov., 4, 956, 10.1158/2159-8290.CD-13-0879

Gawad, 2014, Dissecting the clonal origins of childhood acute lymphoblastic leukemia by single-cell genomics, Proc. Natl. Acad. Sci. U. S. A., 111, 17947, 10.1073/pnas.1420822111

Baslan, 2015, Optimizing sparse sequencing of single cells for highly multiplex copy number profiling, Genome Res., 125, 714, 10.1101/gr.188060.114

Hughes, 2014, Clonal architecture of secondary acute myeloid leukemia defined by single-cell sequencing, PLoS Genet., 10, e1004462, 10.1371/journal.pgen.1004462

Kuipers, 2017, Advances in understanding tumour evolution through single-cell sequencing, Biochim. Biophys. Acta - Rev. Cancer, 1867, 127, 10.1016/j.bbcan.2017.02.001

Hou, 2012, Single-cell exome sequencing and monoclonal evolution of a JAK2-negative myeloproliferative neoplasm, Cell, 148, 873, 10.1016/j.cell.2012.02.028

Woodworth, 2017, Building a lineage from single cells: genetic techniques for cell lineage tracking, Nat. Rev. Genet., 18, 230, 10.1038/nrg.2016.159

Phesse, 2017, Defining key concepts of intestinal and epithelial cancer biology through the use of mouse models, Carcinogenesis, 38, 953, 10.1093/carcin/bgx080

Thliveris, 2011, Clonal structure of carcinogen-induced intestinal tumors in mice, Cancer Prevent. Res., 4, 916, 10.1158/1940-6207.CAPR-11-0022

Thliveris, 2013, Transformation of epithelial cells through recruitment leads to polyclonal intestinal tumors, Proc. Natl. Acad. Sci. U. S. A., 110, 11523, 10.1073/pnas.1303064110

Ellenbroek, 2014, Imaging hallmarks of cancer in living mice, Nat. Rev. Cancer, 14, 406, 10.1038/nrc3742

Zahm, 2016, Advanced intestinal cancers often maintain a multi-ancestral architecture, PLoS One, 11, e0150170, 10.1371/journal.pone.0150170

Leystra, 2016, Abstract 2381: a multiancestral model of colorectal cancer: &em&in vivo&/em& evidence that early heterogeneity contributes to cancer progression, Cancer Res., 76, 2381, 10.1158/1538-7445.AM2016-2381

Schepers, 2012, Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas, Science, 337, 730, 10.1126/science.1224676

Tanaka, 2016, Bmi1-positive cells in the lingual epithelium could serve as cancer stem cells in tongue cancer, Sci. Rep., 6, 39386, 10.1038/srep39386

Yanai, 2017, Intestinal cancer stem cells marked by Bmi1 or Lgr5 expression contribute to tumor propagation via clonal expansion, Sci. Rep., 7, 41838, 10.1038/srep41838

McCreery, 2016, Clonal evolution of skin carcinomas during tumor progression and metastasis, Cancer Res., 76, 2376, 10.1158/1538-7445.AM2016-2376

Maddipati, 2015, Pancreatic cancer metastases harbor evidence of polyclonality, Cancer Discov., 5, 1086, 10.1158/2159-8290.CD-15-0120

Lafaro, 2015, Clonal composition and clonal selection during PanIN progression, Cancer Res., 75, PR04, 10.1158/1538-7445.PANCA2014-PR04

Fischer, 2014, Occult progression by Apc-deficient intestinal crypts as a target for chemoprevention, Carcinogenesis, 35, 237, 10.1093/carcin/bgt296

Dakubo, 2015, Slaughters field cancerization concept of carcinogenesis: the path forward to early cancer detection and chemoprevention, Cell Dev. Biol., 4, 158, 10.4172/2168-9296.1000158

Lochhead, 2015, Etiologic field effect: reappraisal of the field effect concept in cancer predisposition and progression, Mod. Pathol., 28, 14, 10.1038/modpathol.2014.81

Graham, 2011, Field cancerization in the GI tract, Future Oncol., 7, 981, 10.2217/fon.11.70

Marusyk, 2012, Intra-tumour heterogeneity: a looking glass for cancer?, Nat. Rev. Cancer, 12, 323, 10.1038/nrc3261

Woodman, 2010, Are oncogenes sufficient to cause human cancer?, Proc. Natl. Acad. Sci. U. S. A., 107, 20599, 10.1073/pnas.1015563107

Davis, 2017, Tumor evolution: linear, branching, neutral or punctuated?, Biochim. Biophys. Acta (BBA) - Rev. Cancer, 1867, 151, 10.1016/j.bbcan.2017.01.003

Parsons, 2010, Oncomutations as biomarkers of cancer risk, Environ. Mol. Mutagen., 51, 836, 10.1002/em.20600

Parsons, 2017, Variation in organ-specific PIK3CA and KRAS mutant levels in normal human tissues correlates with mutation prevalence in corresponding carcinomas, Environ. Mol. Mutagen., 58, 466, 10.1002/em.22110

Sudo, 2008, Fetal–juvenile origins of point mutations in the adult human tracheal–bronchial epithelium: absence of detectable effects of age, gender or smoking status, Mutat. Res./Fundam. Mol. Mech. Mutagen., 646, 25, 10.1016/j.mrfmmm.2008.08.016

Gao, 2017, KRAS and TP53 mutations in bronchoscopy samples from former lung cancer patients, Mol. Carcinog., 56, 381, 10.1002/mc.22501

Michor, 2010, The origins and implications of intratumor heterogeneity, Cancer Prevent. Res., 3, 1361, 10.1158/1940-6207.CAPR-10-0234

Neelakantan, 2015, Intratumoral heterogeneity: clonal cooperation in epithelial-to-mesenchymal transition and metastasis, Cell Adhes. Migr., 9, 265, 10.4161/19336918.2014.972761

Kalluri, 2009, The basics of epithelial-mesenchymal transition, J. Clin. Invest., 119, 1420, 10.1172/JCI39104

Chaffer, 2011, Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state, Proc. Natl. Acad. Sci. U. S. A., 108, 7950, 10.1073/pnas.1102454108

Köhler, 2017, Mouse cutaneous melanoma induced by mutant BRaf arises from expansion and dedifferentiation of mature pigmented melanocytes, Cell Stem Cell, 21, 679, 10.1016/j.stem.2017.08.003

Graham, 2008, Investigating the fixation and spread of mutations in the gastrointestinal epithelium, Future Oncol., 4, 825, 10.2217/14796694.4.6.825

Tabassum, 2015, Tumorigenesis: it takes a village, Nat. Rev. Cancer, 15, 473, 10.1038/nrc3971

Ramón y Cajal, 2017, Cancer as an ecomolecular disease and a neoplastic consortium, Biochim. Biophys. Acta - Rev. Cancer, 1868, 484, 10.1016/j.bbcan.2017.09.004

McGranahan, 2017, Clonal heterogeneity and tumor evolution: past, present, and the future, Cell, 168, 613, 10.1016/j.cell.2017.01.018

Ge, 2010, Could stroma contribute to field cancerization?, Med. Hypotheses, 75, 26, 10.1016/j.mehy.2010.01.019

Soto, 2011, The tissue organization field theory of cancer: a testable replacement for the somatic mutation theory, BioEssays, 33, 332, 10.1002/bies.201100025

Wu, 2010, Interaction between RasV12 and scribbled clones induces tumour growth and invasion, Nature, 463, 545, 10.1038/nature08702

Cleary, 2014, Tumour cell heterogeneitymaintained by cooperating subclones in Wnt-driven mammary cancers, Nature, 509, 113, 10.1038/nature13187

Inda, 2010, Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma, Genes Dev., 24, 1731, 10.1101/gad.1890510

Bailey, 2016, P53 mutations cooperate with oncogenic Kras to promote adenocarcinoma from pancreatic ductal cells, Oncogene, 35, 4282, 10.1038/onc.2015.441

Casás-Selves, 2011, How cancer shapes evolution, and how evolution shapes cancer, Evolution, 4, 624

Hafner, 2010, Multiple oncogenic mutations and clonal relationship in spatially distinct benign human epidermal tumors, Proc. Natl. Acad. Sci. U. S. A., 107, 20780, 10.1073/pnas.1008365107

Liou, 2016, Mutant KRas-Induced mitochondrial oxidative stress in acinar cells upregulates EGFR signaling to drive formation of pancreatic precancerous lesions, Cell Rep., 14, 2325, 10.1016/j.celrep.2016.02.029

Sievers, 2016, Subclonal diversity arises early even in small colorectal tumours and contributes to differential growth fates, Gut, 66

Sievers, 2017, New insights into the earliest stages of colorectal tumorigenesis, Expert Rev. Gastroenterol. Hepatol., 11, 723, 10.1080/17474124.2017.1330150

Fisher, 2013, Cancer heterogeneity: implications for targeted therapeutics, Br. J. Cancer, 108, 479, 10.1038/bjc.2012.581

Rozhok, 2015, Toward an evolutionary model of cancer: considering the mechanisms that govern the fate of somatic mutations, Proc. Natl. Acad. Sci. U. S. A., 112, 8914, 10.1073/pnas.1501713112

Wu, 2016, Substantial contribution of extrinsic risk factors to cancer development, Nature, 529, 43, 10.1038/nature16166

Fearon, 1990, A genetic model for colorectal tumorigenesis, Cell, 61, 759, 10.1016/0092-8674(90)90186-I

Sottoriva, 2015, A Big Bang model of human colorectal tumor growth, Nat. Genet., 47, 209, 10.1038/ng.3214

Cross, 2016, New paradigms in clonal evolution: punctuated equilibrium in cancer, J. Pathol., 240, 126, 10.1002/path.4757

Sievers, 2016, Understanding intratumoral heterogeneity: lessons from the analysis of at-risk tissue and premalignant lesions in the colon, Cancer Prevent. Res., 9, 638, 10.1158/1940-6207.CAPR-16-0096

Gao, 2016, Punctuated copy number evolution and clonal stasis in triple-negative breast cancer, Nat. Genet., 48, 1119, 10.1038/ng.3641

Beckman, 2017, Evolutionary dynamics and significance of multiple subclonal mutations in cancer, DNA Repair, 56, 7, 10.1016/j.dnarep.2017.06.002

Nicholson, 2018, Fixation and spread of somatic clones in adult human colonic epithelium, Cell Stem Cell, 10.1016/j.stem.2018.04.020

Tomlinson, 2001, Mutations in normal breast tissue and breast tumours, Breast Cancer Res., 3, 299, 10.1186/bcr311

Huang, 2014, Oncogenic K-Ras requires activation for enhanced activity, Oncogene, 33, 532, 10.1038/onc.2012.619

Martincorena, 2015, Somatic mutation in cancer and normal cells, Science, 349, 1483, 10.1126/science.aab4082

Tomasetti, 2017, Stem cell divisions, somatic mutations, cancer etiology, and cancer prevention, Science, 355, 1330, 10.1126/science.aaf9011

Tomasetti, 2015, Variation in cancer risk among tissues can be explained by the number of stem cell divisions, Science, 347, 78, 10.1126/science.1260825

Zhu, 2017, Contributions of the intrinsic mutation process to cancer mutation and risk burdens, EBioMedicine, 24, 5, 10.1016/j.ebiom.2017.09.026

Sudo, 2008, Fetal-juvenile origins of point mutations in the adult human tracheal-bronchial epithelium: absence of detectable effects of age, gender or smoking status, Mutat. Res. - Fundam. Mol. Mech. Mutagen., 646, 25, 10.1016/j.mrfmmm.2008.08.016

Calabrese, 2013, Origin of the linearity no threshold (LNT) dose–response concept, Arch. Toxicol., 87, 1621, 10.1007/s00204-013-1104-7

Gong, 2009, Clonal status and clinicopathological feature of Erdheim-Chester disease, Pathol. Res. Pract., 205, 601, 10.1016/j.prp.2009.02.004

Josten, 1991, Acquired aplastic anemia and paroxysmal nocturnal hemoglobinuria: studies on clonality, Blood, 78, 3162, 10.1182/blood.V78.12.3162.3162

Beer, 2009, Clonal diversity in the myeloproliferative neoplasms: independent origins of genetically distinct clones, Br. J. Haematol., 144, 904, 10.1111/j.1365-2141.2008.07560.x

Takatsu, 2013, Clonality analysis suggests that STK11 gene mutations are involved in progression of lobular endocervical glandular hyperplasia (LEGH) to minimal deviation adenocarcinoma (MDA), Virchows Arch., 462, 645, 10.1007/s00428-013-1417-1

Almeida, 2014, Increased expression of ACTH (MC2R) and androgen (AR) receptors in giant bilateral myelolipomas from patients with congenital adrenal hyperplasia, BMC Endocr. Disord., 14, 42, 10.1186/1472-6823-14-42

Allen, 2014, X chromosome inactivation analysis reveals a difference in the biology of ET patients with JAK2 and CALR mutations, Blood, 124, 2091, 10.1182/blood-2014-06-580183

Kum, 2011, Mixed epithelial and stromal tumors of the kidney: evidence for a single cell of origin with capacity for epithelial and stromal differentiation, Am. J. Surg. Pathol., 35, 1114, 10.1097/PAS.0b013e3182233fb6

Wang, 2009, Evidence for common clonal origin of multifocal lung cancers, J. Natl. Cancer Inst., 101, 560, 10.1093/jnci/djp054

Wang, 2016, Clonality assessment of adenomatoid tumor supports its neoplastic nature, Hum. Pathol., 48, 88, 10.1016/j.humpath.2015.09.032

Gomes, 2009, Clonal nature of odontogenic tumours, J. Oral Pathol. Med., 38, 397, 10.1111/j.1600-0714.2008.00744.x

Emerson, 2007, Molecular genetic evidence supporting the neoplastic nature of the Leydig cell component of ovarian Sertoli-Leydig cell tumors, Int. J. Gynecol. Pathol., 26, 368, 10.1097/pgp.0b013e31802f3100

Singhi, 2013, Acinar cell cystadenoma of the pancreas a benign neoplasm or non-neoplastic ballooning of acinar and ductal epithelium, Am. J. Surg. Pathol., 37, 1329, 10.1097/PAS.0b013e3182a1ad72

Van Egmond, 2013, Monoclonal origin of primary unilateral multifocal pleomorphic adenoma of the parotid gland, Hum. Pathol., 44, 923, 10.1016/j.humpath.2012.10.008

Chiu, 2011, Clonal X-chromosome inactivation suggests that splenic cord capillary hemangioma is a true neoplasm and not a subtype of splenic hamartoma, Mod. Pathol., 24, 108, 10.1038/modpathol.2010.168

Bourdeaut, 2008, In neuroblastic tumours, Schwann cells do not harbour the genetic alterations of neuroblasts but may nevertheless share the same clonal origin, Oncogene, 27, 3066, 10.1038/sj.onc.1210965

Holdsworth-Carson, 2014, Clonality of smooth muscle and fibroblast cell populations isolated from human fibroid and myometrial tissues, Mol. Hum. Reprod., 20, 250, 10.1093/molehr/gat083

Sung, 2007, Histogenesis of sarcomatoid urothelial carcinoma of the urinary bladder: evidence for a common clonal origin with divergent differentiation, J. Pathol., 211, 420, 10.1002/path.2129

Sarubi, 2001, Clonal composition of human adamantinomatous craniopharyngiomas and somatic mutation analyses of the patched (PTCH), Gsα and Gi2α genes, Neurosci. Lett., 310, 5, 10.1016/S0304-3940(01)02048-1

Zhang, 2014, Axillary metaplastic breast carcinoma with ipsilateral pectoral invasive ductal carcinoma: an unusual presentation, Case Rep. Oncol. Med., 2014, 938509

Hodges, 2010, Clonal origin of multifocal hepatocellular carcinoma, Cancer, 116, 4078, 10.1002/cncr.25258

Comertpay, 2014, Evaluation of clonal origin of malignant mesothelioma, J. Transl. Med., 12, 301, 10.1186/s12967-014-0301-3

Yuan, 2015, Use of X-Chromosome inactivation pattern to analyze the clonality of 14 female cases of Kaposi Sarcoma, Med. Sci. Monit. Basic Res., 21, 116, 10.12659/MSMBR.894089

Bahrami, 2007, Clonal relationships between epidermotropic metastatic melanomas and their primary lesions: a loss of heterozygosity and X-chromosome inactivation-based analysis, Mod. Pathol., 20, 821, 10.1038/modpathol.3800833

Katona, 2007, Genetically heterogeneous and clonally unrelated metastases may arise in patients with cutaneous melanoma, Am. J. Surg. Pathol., 31, 1029, 10.1097/PAS.0b013e31802b3488

Nakazawa, 2015, Multicentric occurrence of multiple papillary thyroid carcinomas -HUMARA and BRAF mutation analysis, Cancer Med., 4, 1272, 10.1002/cam4.466

Gong, 2011, Determination of clonal status of pulmonary sclerosing hemangioma with X-chromosome inactivation mosaicism and polymorphism of phosphoglycerate kinase and androgen receptor genes, Med. Oncol., 28, 913, 10.1007/s12032-010-9539-7

Wang, 2015, Clonality analysis of combined Brenner and mucinous tumours of the ovary reveals their monoclonal origin, J. Pathol., 237, 146, 10.1002/path.4572

Karino, 2016, Clonality analysis performed using human androgen receptor assay in a rare case of undifferentiated thymic carcinoma coexisting with type AB thymoma, Pathol. Int., 66, 398, 10.1111/pin.12426

Lin, 2014, Pelvic intravascular leiomyomatosis associated with benign pulmonary metastasizing leiomyoma: clinicopathologic, clonality, and copy number variance analysis, Int. J. Gynecol. Pathol., 33, 140, 10.1097/PGP.0b013e31828def26

Cai, 2007, X-chromosomal inactivation analysis of uterine leiomyomas reveals a common clonal origin of different tumor nodules in some multiple leiomyomas, Int. J. Oncol., 31, 1379

Tazaki, 2013, Histopathologcial and clonal study of combined lobular and ductal carcinoma of the breast, Pathol. Int., 63, 297, 10.1111/pin.12065

Gong, 2009, c-KIT gene mutation and clonal origin of multiple gastrointestinal stromal tumors occurring in the peritoneum, Mol. Med. Rep., 2, 999

Cheng, 2008, Evidence for polyclonal origin of multifocal clear cell renal cell carcinoma, Clin. Cancer Res., 14, 8087, 10.1158/1078-0432.CCR-08-1494

Sung, 2008, Histogenesis of clear cell adenocarcinoma in the urinary tract: evidence of urothelial origin, Clin. Cancer Res., 14, 1947, 10.1158/1078-0432.CCR-07-4147

Williamson, 2013, Malignant perivascular epithelioid cell neoplasm (PEComa) of the urinary bladder with TFE3 gene rearrangement clinicopathologic, immunohistochemical, and molecular features, Am. J. Surg. Pathol., 37, 1619, 10.1097/PAS.0b013e318293729d

Graham, 2010, Investigating clonal competition in barrett’s associated tumorigenesis using spatial maps of genetic heterogeneity, Gut, 59, A111, 10.1136/gut.2009.208983i

Thirlwell, 2010, Clonality assessment and clonal ordering of individual neoplastic crypts shows polyclonality of colorectal adenomas, Gastroenterology, 138, 1441, 10.1053/j.gastro.2010.01.033

Navin, 2010, Inferring tumor progression from genomic heterogeneity, Genome Res., 20, 68, 10.1101/gr.099622.109

Gutierrezgonzalez, 2011, The clonal origins of dysplasia from intestinal metaplasia in the human stomach, Gastroenterology, 140, 1251, 10.1053/j.gastro.2010.12.051

Ventayol Garcia, 2012, The clonal origins of gastric adenocarcinoma, Gut, 61, A43

Waanders, 2012, The origin and nature of tightly clustered BTG1 deletions in precursor B-cell acute lymphoblastic leukemia support a model of multiclonal evolution, PLoS Genet., 8, e1002533, 10.1371/journal.pgen.1002533

Walter, 2012, Clonal architecture of secondary acute myeloid leukemia, New Engl. J. Med., 366, 1090, 10.1056/NEJMoa1106968

Zeki, 2012, Barretts related adenocarcinomas arise as a monoclonal outgrowth from polyclonal dysplasia, Gastroenterology, 142, S643, 10.1016/S0016-5085(12)62478-0

Weaver, 2014, Ordering of mutations in preinvasive disease stages of esophageal carcinogenesis, Nat. Genet., 46, 837, 10.1038/ng.3013

Li, 2014, A general framework for analyzing tumor subclonality using SNP array and DNA sequencing data, Genome Biol., 15, 473, 10.1186/s13059-014-0473-4

Gu, 2015, Hepatic carcinosarcoma: evidence of polyclonal origin based on microsatellite analysis, Pathol. Res. Pract., 211, 905, 10.1016/j.prp.2015.09.007

Boutros, 2015, Spatial genomic heterogeneity within localized, multifocal prostate cancer, Nat. Genet., 47, 736, 10.1038/ng.3315

Gomes, 2016, Intratumor molecular heterogeneity in pleomorphic adenoma of the salivary glands, Oral. Surg. Oral Med. Oral Pathol. Oral Radiol., 121, 158, 10.1016/j.oooo.2015.09.007

Cereda, 2016, Patients with genetically heterogeneous synchronous colorectal cancer carry rare damaging germline mutations in immune-related genes, Nat. Commun., 7, 10.1038/ncomms12072

Gausachs, 2017, Mutational heterogeneity in APC and KRAS arises at the crypt level and leads to polyclonality in early colorectal tumorigenesis, Clin. Cancer Res., 23, 5936, 10.1158/1078-0432.CCR-17-0821

Baker, 2017, Visualization of treatment resistant subclones in colorectal cancer by mutation specific RNA in situ hybridization, Cancer Res., 77, 3953, 10.1158/1538-7445.AM2017-3953

Navin, 2011, Tumour evolution inferred by single-cell sequencing, Nature, 472, 90, 10.1038/nature09807

Xu, 2012, Single-cell exome sequencing reveals single-nucleotide mutation characteristics of a kidney tumor, Cell, 148, 886, 10.1016/j.cell.2012.02.025

Li, 2012, Single-cell sequencing analysis characterizes common and cell-lineage-specific mutations in a muscle-invasive bladder cancer, GigaScience, 1, 12, 10.1186/2047-217X-1-12

Patel, 2014, Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma, Science, 344, 1396, 10.1126/science.1254257

Knudson, 1973, Mutation and human cancer, Adv. Cancer Res., 17, 317, 10.1016/S0065-230X(08)60534-5

Nowell, 1976, The clonal evolution of tumor cell populations. Acquired genetic lability permits stepwise selection of variant sublines and underlies tumor progression, Science, 194, 23, 10.1126/science.959840

Fearon, 1987, Clonal analysis of human colorectal tumors, Science, 238, 193, 10.1126/science.2889267

Vogelstein, 1985, Use of restriction fragment length polymorphisms to determine the clonal origin of human tumors, Science, 227, 642, 10.1126/science.2982210

Lyon, 1961, Gene action in the x-chromosome of the mouse (Mus Musculus L.), Nature, 190, 372, 10.1038/190372a0

Linder, 1965, Glucose-6-phosphate dehydrogenase mosaicism: utilization as a cell marker in the study of leiomyomas, Science, 150, 67, 10.1126/science.150.3692.67

Fialkow, 1971, Multiple cell origin of hereditary neurofibromas, N. Engl. J. Med., 284, 296, 10.1056/NEJM197102112840604