Parallel Progression of Primary Tumours and Metastases

Overview

Journal Nat Rev Cancer

Specialty Oncology

Date 2009 Mar 25

PMID 19308069

Citations 524

Authors

Christoph A Klein

Affiliations

Soon will be listed here.

Abstract

Systemic cancer progression is accounted for in two basic models. The prevailing archetype places the engine of cancer progression within the primary tumour before metastatic dissemination of fully malignant cells. The second posits parallel, independent progression of metastases arising from early disseminated tumour cells. This Perspective draws together data from disease courses, tumour growth rates, autopsy studies, clinical trials and molecular genetic analyses of primary and disseminated tumour cells in support of the parallel progression model. Consideration of this model urges review of current diagnostic and therapeutic routines.

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References

Cheng L, Pisansky T, Sebo T, Leibovich B, Ramnani D, Weaver A . Cell proliferation in prostate cancer patients with lymph node metastasis: a marker for progression. Clin Cancer Res. 1999; 5(10):2820-3. View

McAllister S, Gifford A, Greiner A, Kelleher S, Saelzler M, Ince T . Systemic endocrine instigation of indolent tumor growth requires osteopontin. Cell. 2008; 133(6):994-1005. PMC: 4121664. DOI: 10.1016/j.cell.2008.04.045. View

Arteaga C, Baselga J . Tyrosine kinase inhibitors: why does the current process of clinical development not apply to them?. Cancer Cell. 2004; 5(6):525-31. DOI: 10.1016/j.ccr.2004.05.028. View

Solakoglu O, Maierhofer C, Lahr G, Breit E, Scheunemann P, Heumos I . Heterogeneous proliferative potential of occult metastatic cells in bone marrow of patients with solid epithelial tumors. Proc Natl Acad Sci U S A. 2002; 99(4):2246-51. PMC: 122350. DOI: 10.1073/pnas.042372199. View

Pantel K, Schlimok G, Braun S, Kutter D, Lindemann F, Schaller G . Differential expression of proliferation-associated molecules in individual micrometastatic carcinoma cells. J Natl Cancer Inst. 1993; 85(17):1419-24. DOI: 10.1093/jnci/85.17.1419. View

Klein C, Schardt J, Pantel K, Speicher M, Riethmuller G . Comparative genomic hybridization, loss of heterozygosity, and DNA sequence analysis of single cells. Proc Natl Acad Sci U S A. 1999; 96(8):4494-9. PMC: 16360. DOI: 10.1073/pnas.96.8.4494. View

Spratt J, Meyer J, Spratt J . Rates of growth of human neoplasms: Part II. J Surg Oncol. 1996; 61(1):68-83. DOI: 10.1002/1096-9098(199601)61:1<68::aid-jso2930610102>3.0.co;2-e. View

Kang Y, Siegel P, Shu W, Drobnjak M, Kakonen S, Cordon-Cardo C . A multigenic program mediating breast cancer metastasis to bone. Cancer Cell. 2003; 3(6):537-49. DOI: 10.1016/s1535-6108(03)00132-6. View

Cristofanilli M, Budd G, Ellis M, Stopeck A, Matera J, Miller M . Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med. 2004; 351(8):781-91. DOI: 10.1056/NEJMoa040766. View

10.

Baudis M . Genomic imbalances in 5918 malignant epithelial tumors: an explorative meta-analysis of chromosomal CGH data. BMC Cancer. 2007; 7:226. PMC: 2225423. DOI: 10.1186/1471-2407-7-226. View

11.

Fidler I . Selection of successive tumour lines for metastasis. Nat New Biol. 1973; 242(118):148-9. DOI: 10.1038/newbio242148a0. View

12.

Badalian G, Barbai T, Raso E, Derecskei K, Szendroi M, Timar J . Phenotype of bone metastases of non-small cell lung cancer: epidermal growth factor receptor expression and K-RAS mutational status. Pathol Oncol Res. 2007; 13(2):99-104. DOI: 10.1007/BF02893484. View

13.

Fiegler H, Geigl J, Langer S, Rigler D, Porter K, Unger K . High resolution array-CGH analysis of single cells. Nucleic Acids Res. 2006; 35(3):e15. PMC: 1807964. DOI: 10.1093/nar/gkl1030. View

14.

Rudenstam C, Zahrieh D, Forbes J, Crivellari D, Holmberg S, Rey P . Randomized trial comparing axillary clearance versus no axillary clearance in older patients with breast cancer: first results of International Breast Cancer Study Group Trial 10-93. J Clin Oncol. 2005; 24(3):337-44. DOI: 10.1200/JCO.2005.01.5784. View

15.

Kitchener H, Swart A, Qian Q, Amos C, Parmar M . Efficacy of systematic pelvic lymphadenectomy in endometrial cancer (MRC ASTEC trial): a randomised study. Lancet. 2008; 373(9658):125-36. PMC: 2646126. DOI: 10.1016/S0140-6736(08)61766-3. View

16.

Quintana E, Shackleton M, Sabel M, Fullen D, Johnson T, Morrison S . Efficient tumour formation by single human melanoma cells. Nature. 2008; 456(7222):593-8. PMC: 2597380. DOI: 10.1038/nature07567. View

17.

Artale S, Sartore-Bianchi A, Veronese S, Gambi V, Sarnataro C, Gambacorta M . Mutations of KRAS and BRAF in primary and matched metastatic sites of colorectal cancer. J Clin Oncol. 2008; 26(25):4217-9. DOI: 10.1200/JCO.2008.18.7286. View

18.

van de Wouw A, Janssen-Heijnen M, Coebergh J, Hillen H . Epidemiology of unknown primary tumours; incidence and population-based survival of 1285 patients in Southeast Netherlands, 1984-1992. Eur J Cancer. 2002; 38(3):409-13. DOI: 10.1016/s0959-8049(01)00378-1. View

19.

Viadana E, Cotter R, PICKREN J, Bross I . An autopsy study of metastatic sites of breast cancer. Cancer Res. 1973; 33(1):179-81. View

20.

Albanese I, Scibetta A, Migliavacca M, Russo A, Bazan V, Tomasino R . Heterogeneity within and between primary colorectal carcinomas and matched metastases as revealed by analysis of Ki-ras and p53 mutations. Biochem Biophys Res Commun. 2004; 325(3):784-91. DOI: 10.1016/j.bbrc.2004.10.111. View