#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Fiber stiffness, pore size and adhesion control migratory phenotype of MDA-MB-231 cells in collagen gels


Autoři: Florian Geiger aff001;  Daniel Rüdiger aff002;  Stefan Zahler aff002;  Hanna Engelke aff001
Působiště autorů: Department of Chemistry and Center for NanoScience, Ludwig-Maximilians-Universität München, Munich, Germany aff001;  Department of Pharmacy, Ludwig-Maximilians-Universität München, Munich, Germany aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0225215

Souhrn

Cancer cell migration is influenced by cellular phenotype and behavior as well as by the mechanical and chemical properties of the environment. Furthermore, many cancer cells show plasticity of their phenotype and adapt it to the properties of the environment. Here, we study the influence of fiber stiffness, confinement, and adhesion properties on cancer cell migration in porous collagen gels. Collagen gels with soft fibers abrogate migration and promote a round, non-invasive phenotype. Stiffer collagen fibers are inherently more adhesive and lead to the existence of an adhesive phenotype and in general confined migration due to adhesion. Addition of TGF-β lowers adhesion, eliminates the adhesive phenotype and increases the amount of highly motile amoeboid phenotypes. Highest migration speeds and longest displacements are achieved in stiff collagen fibers in pores of about cell size by amoeboid phenotypes. This elucidates the influence of the mechanical properties of collagen gels on phenotype and subsequently migration and shows that stiff fibers, cell sized pores, and low adhesion, are optimal conditions for an amoeboid phenotype and efficient migration.

Klíčová slova:

Adhesives – Collagens – Fluorescence imaging – Stiffness – Statistical distributions – Gels – Cell migration – Cancer cell migration


Zdroje

1. Charras G, Sahai E. Physical influences of the extracellular environment on cell migration. Nat Rev Mol Cell Biol. 2014;15(12):813–24. doi: 10.1038/nrm3897 25355506

2. Ruprecht V, Monzo P, Ravasio A, Yue Z, Makhija E, Strale PO, et al. How cells respond to environmental cues—insights from bio-functionalized substrates. J Cell Sci. 2017;130(1):51–61. doi: 10.1242/jcs.196162 27856508

3. Caswell PT, Zech T. Actin-Based Cell Protrusion in a 3D Matrix. Trends Cell Biol. 2018;28(10):823–34. doi: 10.1016/j.tcb.2018.06.003 29970282

4. Harley BA, Kim HD, Zaman MH, Yannas IV, Lauffenburger DA, Gibson LJ. Microarchitecture of three-dimensional scaffolds influences cell migration behavior via junction interactions. Biophys J. 2008;95(8):4013–24. doi: 10.1529/biophysj.107.122598 18621811

5. Wu P-H, Gilkes DM, Wirtz D. The Biophysics of 3D Cell Migration. Annu Rev Biophys. 2018;47(1):549–67.

6. Wolf K, Te Lindert M, Vortmeyer, Alexander S, te Riet J, L Willis A, et al. Physical limits of cell migration: Control by ECM space and nuclear deformation and tuning by proteolysis and traction force2013. 1069–84 p.

7. Lammermann T, Bader BL, Monkley SJ, Worbs T, Wedlich-Soldner R, Hirsch K, et al. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature. 2008;453(7191):51–5. doi: 10.1038/nature06887 18451854

8. Bergert M, Chandradoss SD, Desai RA, Paluch E. Cell mechanics control rapid transitions between blebs and lamellipodia during migration. Proc Natl Acad Sci USA. 2012;109(36):14434–9. doi: 10.1073/pnas.1207968109 22786929

9. Renkawitz J, Schumann K, Weber M, Lammermann T, Pflicke H, Piel M, et al. Adaptive force transmission in amoeboid cell migration. Nat Cell Biol. 2009;11(12):1438–43. doi: 10.1038/ncb1992 19915557

10. Liu YJ, Le Berre M, Lautenschlaeger F, Maiuri P, Callan-Jones A, Heuze M, et al. Confinement and low adhesion induce fast amoeboid migration of slow mesenchymal cells. Cell. 2015;160(4):659–72. doi: 10.1016/j.cell.2015.01.007 25679760

11. Kick K, Nekolla K, Rehberg M, Vollmar AM, Zahler S. New View on Endothelial Cell Migration: Switching Modes of Migration Based on Matrix Composition. Arterioscler Thromb Vasc Biol. 2016;36(12):2346–57. doi: 10.1161/ATVBAHA.116.307870 27737863

12. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, et al. Tensional homeostasis and the malignant phenotype. Cancer Cell. 2005;8(3):241–54. doi: 10.1016/j.ccr.2005.08.010 16169468

13. Holle AW, Govindan Kutty Devi N, Clar K, Fan A, Saif T, Kemkemer R, et al. Cancer Cells Invade Confined Microchannels via a Self-Directed Mesenchymal-to-Amoeboid Transition. Nano Lett. 2019;19(4):2280–90. doi: 10.1021/acs.nanolett.8b04720 30775927

14. Anguiano M, Castilla C, Maska M, Ederra C, Pelaez R, Morales X, et al. Characterization of three-dimensional cancer cell migration in mixed collagen-Matrigel scaffolds using microfluidics and image analysis. PLoS One. 2017;12(2):e0171417. doi: 10.1371/journal.pone.0171417 28166248

15. Talkenberger K, Cavalcanti-Adam EA, Voss-Bohme A, Deutsch A. Amoeboid-mesenchymal migration plasticity promotes invasion only in complex heterogeneous microenvironments. Scientific reports. 2017;7(1):9237. doi: 10.1038/s41598-017-09300-3 28835679

16. Vader D, Kabla A, Weitz D, Mahadevan L. Strain-induced alignment in collagen gels. PLoS One. 2009;4(6):e5902. doi: 10.1371/journal.pone.0005902 19529768

17. Wisdom KM, Adebowale K, Chang J, Lee JY, Nam S, Desai R, et al. Matrix mechanical plasticity regulates cancer cell migration through confining microenvironments. Nat Commun. 2018;9(1):4144. doi: 10.1038/s41467-018-06641-z 30297715

18. Dietrich M, Le Roy H, Bruckner DB, Engelke H, Zantl R, Radler JO, et al. Guiding 3D cell migration in deformed synthetic hydrogel microstructures. Soft Matter. 2018;14(15):2816–26. doi: 10.1039/c8sm00018b 29595213

19. Wu PH, Giri A, Sun SX, Wirtz D. Three-dimensional cell migration does not follow a random walk. Proc Natl Acad Sci USA. 2014;111(11):3949–54. doi: 10.1073/pnas.1318967111 24594603

20. Wolf K, Alexander S, Schacht V, Coussens LM, von Andrian UH, van Rheenen J, et al. Collagen-based cell migration models in vitro and in vivo. Semin Cell Dev Biol. 2009;20(8):931–41. doi: 10.1016/j.semcdb.2009.08.005 19682592

21. Provenzano PP, Eliceiri KW, Campbell JM, Inman DR, White JG, Keely PJ. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med. 2006;4(1):38. doi: 10.1186/1741-7015-4-38 17190588

22. Sauer F, Oswald L, Ariza de Schellenberger A, Tzschatzsch H, Schrank F, Fischer T, et al. Collagen networks determine viscoelastic properties of connective tissues yet do not hinder diffusion of the aqueous solvent. Soft Matter. 2019;15(14):3055–64. doi: 10.1039/c8sm02264j 30912548

23. Tozluoglu M, Tournier AL, Jenkins RP, Hooper S, Bates PA, Sahai E. Matrix geometry determines optimal cancer cell migration strategy and modulates response to interventions. Nat Cell Biol. 2013;15(7):751–62. doi: 10.1038/ncb2775 23792690

24. Doyle AD, Carvajal N, Jin A, Matsumoto K, Yamada KM. Local 3D matrix microenvironment regulates cell migration through spatiotemporal dynamics of contractility-dependent adhesions. Nat Commun. 2015;6:8720. doi: 10.1038/ncomms9720 26548801

25. Licup AJ, Münster S, Sharma A, Sheinman M, Jawerth LM, Fabry B, et al. Stress controls the mechanics of collagen networks. Proc Natl Acad Sci USA. 2015;112(31):9573–8. doi: 10.1073/pnas.1504258112 26195769

26. Broda E, Torrano AA, Löbbert L, Möckl L, Bräuchle C, Engelke H. Invasiveness of Cells Leads to Changes in Their Interaction Behavior with the Glycocalyx. Adv Biosyst. 2018;2(8):1800083.

27. Lammermann T, Sixt M. Mechanical modes of 'amoeboid' cell migration. Curr Opin Cell Biol. 2009;21(5):636–44. doi: 10.1016/j.ceb.2009.05.003 19523798

28. Condor M, Mark C, Gerum RC, Grummel NC, Bauer A, Garcia-Aznar JM, et al. Breast Cancer Cells Adapt Contractile Forces to Overcome Steric Hindrance. Biophys J. 2019;116(7):1305–12. doi: 10.1016/j.bpj.2019.02.029 30902366

29. Burov S, Tabei SM, Huynh T, Murrell MP, Philipson LH, Rice SA, et al. Distribution of directional change as a signature of complex dynamics. Proc Natl Acad Sci USA. 2013;110(49):19689–94. doi: 10.1073/pnas.1319473110 24248363

30. Bhowmick NA, Ghiassi M, Bakin A, Aakre M, Lundquist CA, Engel ME, et al. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Molecular biology of the cell. 2001;12(1):27–36. doi: 10.1091/mbc.12.1.27 11160820

31. Sanz-Moreno V, Gadea G, Ahn J, Paterson H, Marra P, Pinner S, et al. Rac activation and inactivation control plasticity of tumor cell movement. Cell. 2008;135(3):510–23. doi: 10.1016/j.cell.2008.09.043 18984162

32. Sahai E, Marshall CJ. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat Cell Biol. 2003;5(8):711–9. doi: 10.1038/ncb1019 12844144

33. Poincloux R, Collin O, Lizárraga F, Romao M, Debray M, Piel M, et al. Contractility of the cell rear drives invasion of breast tumor cells in 3D Matrigel. Proc Natl Acad Sci USA. 2011;108(5):1943–8. doi: 10.1073/pnas.1010396108 21245302

34. Lampi MC, Reinhart-King CA. Targeting extracellular matrix stiffness to attenuate disease: From molecular mechanisms to clinical trials. Science translational medicine. 2018;10(422).

35. Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science. 2005;310(5751):1139–43. doi: 10.1126/science.1116995 16293750

36. Malawista SE, de Boisfleury Chevance A, Boxer LA. Random locomotion and chemotaxis of human blood polymorphonuclear leukocytes from a patient with leukocyte adhesion deficiency-1: normal displacement in close quarters via chimneying. Cell Motil Cytoskeleton. 2000;46(3):183–9. doi: 10.1002/1097-0169(200007)46:3<183::AID-CM3>3.0.CO;2-2 10913965

37. Hawkins RJ, Piel M, Faure-Andre G, Lennon-Dumenil AM, Joanny JF, Prost J, et al. Pushing off the walls: a mechanism of cell motility in confinement. Phys Rev Lett. 2009;102(5):058103. doi: 10.1103/PhysRevLett.102.058103 19257561

38. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–82. doi: 10.1038/nmeth.2019 22743772

39. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–5. doi: 10.1038/nmeth.2089 22930834

40. Doube M, Klosowski MM, Arganda-Carreras I, Cordelieres FP, Dougherty RP, Jackson JS, et al. BoneJ: Free and extensible bone image analysis in ImageJ. Bone. 2010;47(6):1076–9. doi: 10.1016/j.bone.2010.08.023 20817052


Článok vyšiel v časopise

PLOS One


2019 Číslo 11
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#