Stem Cell Control, Oscillations, and Tissue Regeneration in Spatial and Non-spatial Models

Overview

Journal Front Oncol

Specialty Oncology

Date 2013 Apr 19

PMID 23596567

Citations 16

Authors

Ignacio A Rodriguez-Brenes

Dominik Wodarz

Natalia L Komarova

Affiliations

Soon will be listed here.

Abstract

Normal human tissue is organized into cell lineages, in which the highly differentiated mature cells that perform tissue functions are the end product of an orderly tissue-specific sequence of divisions that start with stem cells or progenitor cells. Tissue homeostasis and effective regeneration after injuries requires tight regulation of these cell lineages and feedback loops play a fundamental role in this regard. In particular, signals secreted from differentiated cells that inhibit stem cell division and stem cell self-renewal are important in establishing control. In this article we study in detail the cell dynamics that arise from this control mechanism. These dynamics are fundamental to our understanding of cancer, given that tumor initiation requires an escape from tissue regulation. Knowledge on the processes of cellular control can provide insights into the pathways that lead to deregulation and consequently cancer development.

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References

Piccirillo S, Reynolds B, Zanetti N, Lamorte G, Binda E, Broggi G . Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature. 2006; 444(7120):761-5. DOI: 10.1038/nature05349. View

Al-Hajj M, Wicha M, Benito-Hernandez A, Morrison S, Clarke M . Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003; 100(7):3983-8. PMC: 153034. DOI: 10.1073/pnas.0530291100. View

Michor F, Hughes T, Iwasa Y, Branford S, Shah N, Sawyers C . Dynamics of chronic myeloid leukaemia. Nature. 2005; 435(7046):1267-70. DOI: 10.1038/nature03669. View

Agur Z, Daniel Y, Ginosar Y . The universal properties of stem cells as pinpointed by a simple discrete model. J Math Biol. 2002; 44(1):79-86. DOI: 10.1007/s002850100115. View

Shizuru J, Negrin R, Weissman I . Hematopoietic stem and progenitor cells: clinical and preclinical regeneration of the hematolymphoid system. Annu Rev Med. 2005; 56:509-38. DOI: 10.1146/annurev.med.54.101601.152334. View

Woodford-Richens K, Rowan A, Gorman P, Halford S, Bicknell D, Wasan H . SMAD4 mutations in colorectal cancer probably occur before chromosomal instability, but after divergence of the microsatellite instability pathway. Proc Natl Acad Sci U S A. 2001; 98(17):9719-23. PMC: 55519. DOI: 10.1073/pnas.171321498. View

Elgjo K, Reichelt K . Chalones: from aqueous extracts to oligopeptides. Cell Cycle. 2004; 3(9):1208-11. View

Passegue E, Jamieson C, Ailles L, Weissman I . Normal and leukemic hematopoiesis: are leukemias a stem cell disorder or a reacquisition of stem cell characteristics?. Proc Natl Acad Sci U S A. 2003; 100 Suppl 1:11842-9. PMC: 304096. DOI: 10.1073/pnas.2034201100. View

Nakata Y, Getto P, Marciniak-Czochra A, Alarcon T . Stability analysis of multi-compartment models for cell production systems. J Biol Dyn. 2012; 6 Suppl 1:2-18. DOI: 10.1080/17513758.2011.558214. View

10.

Morrison S, Shah N, Anderson D . Regulatory mechanisms in stem cell biology. Cell. 1997; 88(3):287-98. DOI: 10.1016/s0092-8674(00)81867-x. View

11.

dOnofrio A, Tomlinson I . A nonlinear mathematical model of cell turnover, differentiation and tumorigenesis in the intestinal crypt. J Theor Biol. 2006; 244(3):367-74. DOI: 10.1016/j.jtbi.2006.08.022. View

12.

Adimy M, Crauste F, Ruan S . Modelling hematopoiesis mediated by growth factors with applications to periodic hematological diseases. Bull Math Biol. 2006; 68(8):2321-51. DOI: 10.1007/s11538-006-9121-9. View

13.

McPherron A, Lawler A, Lee S . Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature. 1997; 387(6628):83-90. DOI: 10.1038/387083a0. View

14.

Glauche I, Cross M, Loeffler M, Roeder I . Lineage specification of hematopoietic stem cells: mathematical modeling and biological implications. Stem Cells. 2007; 25(7):1791-9. DOI: 10.1634/stemcells.2007-0025. View

15.

Rodriguez-Brenes I, Komarova N, Wodarz D . Evolutionary dynamics of feedback escape and the development of stem-cell-driven cancers. Proc Natl Acad Sci U S A. 2011; 108(47):18983-8. PMC: 3223454. DOI: 10.1073/pnas.1107621108. View

16.

Neumuller R, Knoblich J . Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev. 2009; 23(23):2675-99. PMC: 2788323. DOI: 10.1101/gad.1850809. View

17.

Ganguly R, Puri I . Mathematical model for the cancer stem cell hypothesis. Cell Prolif. 2006; 39(1):3-14. PMC: 6495990. DOI: 10.1111/j.1365-2184.2006.00369.x. View

18.

Tzeng Y, Li H, Kang Y, Chen W, Cheng W, Lai D . Loss of Cxcl12/Sdf-1 in adult mice decreases the quiescent state of hematopoietic stem/progenitor cells and alters the pattern of hematopoietic regeneration after myelosuppression. Blood. 2010; 117(2):429-39. DOI: 10.1182/blood-2010-01-266833. View

19.

Chou C, Lo W, Gokoffski K, Zhang Y, Wan F, Lander A . Spatial dynamics of multistage cell lineages in tissue stratification. Biophys J. 2010; 99(10):3145-54. PMC: 2980753. DOI: 10.1016/j.bpj.2010.09.034. View

20.

Yatabe Y, Tavare S, Shibata D . Investigating stem cells in human colon by using methylation patterns. Proc Natl Acad Sci U S A. 2001; 98(19):10839-44. PMC: 58561. DOI: 10.1073/pnas.191225998. View