Fibroblast spheroids as a model to study sustained fibroblast quiescence and their crosstalk with tumor cells

Experimental Cell Research

Volumn 345, Issue 1, 2016, Pages 17-24

  Salmenperä, Pertteli ^a   Karhemo, Piia Riitta ^b   Räsänen, Kati ^a   Laakkonen, Pirjo ^b   Vaheri, Antti ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Cellular senescence, quiescence; Fibroblast activation; Nemosis; Secretory phenotype

Indexed keywords

AGAROSE; BETA GALACTOSIDASE; CYTOKERATIN 7; PROTEIN P27; BIOLOGICAL MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CELL CYCLE; CELL FUNCTION; CONTROLLED STUDY; FIBROBLAST; GENE EXPRESSION; GROWTH INHIBITION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MICROARRAY ANALYSIS; MOUSE; MULTICELLULAR SPHEROID; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE; SQUAMOUS CELL CARCINOMA; TUMOR CELL; TUMOR XENOGRAFT; ANIMAL; BIOLOGICAL MODEL; CELL AGING; CELL COMMUNICATION; CELL CYCLE CHECKPOINT; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; KERATINOCYTE; MALE; METABOLISM; NEOPLASM; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; TUMOR CELL LINE;

ANIMALS; BIOMARKERS; CELL AGING; CELL COMMUNICATION; CELL CYCLE; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; FIBROBLASTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; KERATINOCYTES; MALE; MICE, INBRED NOD; MICE, SCID; MODELS, BIOLOGICAL; NEOPLASMS; PHENOTYPE; SPHEROIDS, CELLULAR;

EID: 84971657259     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2016.05.005     Document Type: Article

References (32)

1. Räsänen K., Vaheri A. Activation of fibroblasts in cancer stroma. Exp. Cell Res. 2010, 316:2713-2722.
2. Kalluri R., Zeisberg M. Fibroblasts in cancer. Nat. Rev. Cancer 2006, 6:392-401.
3. Bissell M.J., Hines W.C. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat. Med. 2011, 17:320-329.
4. Coller H.A., Sang L., Roberts J.M. A new description of cellular quiescence. PLoS Biol. 2006, 4:e83.
5. Lemons J.M., Feng X.J., Bennett B.D., Legesse-Miller A., Johnson E.L., Raitman I., Pollina E.A., Rabitz H.A., Rabinowitz J.D., Coller H.A. Quiescent fibroblasts exhibit high metabolic activity. PLoS Biol. 2010, 8:e1000514.
6. Vaheri A., Enzerink A., Räsänen K., Salmenperä P. Nemosis, a novel way of fibroblast activation, in inflammation and cancer. Exp. Cell Res. 2009, 315:1633-1638.
7. Bizik J., Kankuri E., Ristimäki A., Taieb A., Vapaatalo H., Lubitz W., Vaheri A. Cell-cell contacts trigger programmed necrosis and induce cyclooxygenase-2 expression. Cell Death Differ. 2004, 11:183-195.
8. Greenhough A., Smartt H.J., Moore A.E., Roberts H.R., Williams A.C., Paraskeva C., Kaidi A. The COX-2/PGE2 pathway: key roles in the hallmarks of cancer and adaptation to the tumour microenvironment. Carcinogenesis 2009, 30:377-386.
9. Räsänen K., Virtanen I., Salmenperä P., Grenman R., Vaheri A. Differences in the nemosis response of normal and cancer-associated fibroblasts from patients with oral squamous cell carcinoma. PLoS One 2009, 4:e6879.
10. Kankuri E., Cholujova D., Comajova M., Vaheri A., Bizik J. Induction of hepatocyte growth factor/scatter factor by fibroblast clustering directly promotes tumor cell invasiveness. Cancer Res. 2005, 65:9914-9922.
11. Sirén V., Salmenperä P., Kankuri E., Bizik J., Sorsa T., Tervahartiala T., Vaheri A. Cell-cell contact activation of fibroblasts increases the expression of matrix metalloproteinases. Ann. Med. 2006, 38:212-220.
12. Kankuri E., Babusikova O., Hlubinova K., Salmenperä P., Boccaccio C., Lubitz W., Harjula A., Bizik J. Fibroblast nemosis arrests growth and induces differentiation of human leukemia cells. Int. J. Cancer 2008, 122:1243-1252.
13. Enzerink A., Salmenperä P., Kankuri E., Vaheri A. Clustering of fibroblasts induces proinflammatory chemokine secretion promoting leukocyte migration. Mol. Immunol. 2009, 46:1787-1795.
14. Räsänen K., Salmenperä P., Baumann M., Virtanen I., Vaheri A. Nemosis of fibroblasts is inhibited by benign HaCaT keratinocytes but promoted by malignant HaCaT cells. Mol. Oncol. 2008, 2:340-348.
15. Räsänen K., Vaheri A. Proliferation and motility of HaCaT keratinocyte derivatives is enhanced by fibroblast nemosis. Exp. Cell Res. 2010, 316:1739-1747.
16. Fusenig N.E., Boukamp P. Multiple stages and genetic alterations in immortalization, malignant transformation, and tumor progression of human skin keratinocytes. Mol. Carcinog. 1998, 23:144-158.
17. Dimri G.P., Lee X., Basile G., Acosta M., Scott G., Roskelley C., Medrano E.E., Linskens M., Rubelj I., Pereira-Smith O. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 1995, 92:9363-9367.
18. Blomen V.A., Boonstra J. Cell fate determination during G1 phase progression. Cell Mol. Life Sci. 2007, 64:3084-3104.
19. Coppe J.P., Desprez P.Y., Krtolica A., Campisi J. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu. Rev. Pathol. 2010, 5:99-118.
20. von Zglinicki T., Nilsson E., Docke W.D., Brunk U.T. Lipofuscin accumulation and ageing of fibroblasts. Gerontology 1995, 41(Suppl. 2):95-108.
21. Kuilman T., Peeper D.S. Senescence-messaging secretome: SMS-ing cellular stress. Nat. Rev. Cancer 2009, 9:81-94.
22. Xue W., Zender L., Miething C., Dickins R.A., Hernando E., Krizhanovsky V., Cordon-Cardo C., Lowe S.W. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007, 445:656-660.
23. Salmenperä P., Kankuri E., Bizik J., Siren V., Virtanen I., Takahashi S., Leiss M., Fassler R., Vaheri A. Formation and activation of fibroblast spheroids depend on fibronectin-integrin interaction. Exp. Cell Res. 2008, 314:3444-3452.
24. Ha L., Ichikawa T., Anver M., Dickins R., Lowe S., Sharpless N.E., Krimpenfort P., Depinho R.A., Bennett D.C., Sviderskaya E.V., Merlino G. ARF functions as a melanoma tumor suppressor by inducing p53-independent senescence. Proc. Natl. Acad. Sci. USA 2007, 104:10968-10973.
25. Ha L., Ponnamperuma R.M., Jay S., Ricci M.S., Weinberg W.C. Dysregulated DeltaNp63alpha inhibits expression of Ink4a/arf, blocks senescence, and promotes malignant conversion of keratinocytes. PLoS One 2011, 6:e21877.
26. Szabova K., Bizikova I., Mistrik M., Bizik J. Inflammatory environment created by fibroblast aggregates induces growth arrest and phenotypic shift of human myeloma cells. Neoplasma 2015, 62:938-948.
27. Ikeda H., Sasaki M., Sato Y., Harada K., Zen Y., Mitsui T., Nakanuma Y. Bile ductular cell reaction with senescent hepatocytes in chronic viral hepatitis is lost during hepatocarcinogenesis. Pathol. Int. 2009, 59:471-478.
28. Campisi J., d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell Biol. 2007, 8:729-740.
29. Coller H.A. Cell biology. The essence of quiescence. Science 2011, 334:1074-1075.
30. Chen B.R., Cheng H.H., Lin W.C., Wang K.H., Liou J.Y., Chen P.F., Wu K.K. Quiescent fibroblasts are more active in mounting robust inflammatory responses than proliferative fibroblasts. PLoS One 2012, 7:e49232.
31. Blagosklonny M.V. Cell cycle arrest is not senescence. Aging 2011, 3:94-101.
32. Ehrlich H.P., Diez T. Role for gap junctional intercellular communications in wound repair. Wound Repair Regen. 2003, 11:481-489.