Phagocyte architecture and dynamics

Macrophages are innate immune cells that maintain tissue homeostasis and immune surveillance in all tissues, but are also involved in disease progression (such as chronic inflammatory diseases and cancer). A therapeutic strategy is thus to limit tissue infiltration of pathogenic macrophages.

Using intravital microscopy, our team revealed that macrophages use the mesenchymal mode of migration to infiltrate dense tumors and that inhibitors of matrix metalloproteases both decreased the number of tumor-associated macrophages and tumor growth (Gui et al. 2018 Cancer Immunol. Res.). Podosomes are cell adhesion structures involved in the degradation of the extracellular matrix and the mesenchymal migration of macrophages. They are composed of a submicron core of actin filaments surrounded by a ring of integrin-based adhesion complexes.

Thanks to a method that we called protrusion force microscopy, we demonstrated that podosomes generate protrusive forces that are proportional to the stiffness of the extracellular matrix (Labernadie et al. 2014 Nat. Commun.; Proag et al. 2015 ACS Nano), and involve a balance of forces between core protrusion and a traction at the adhesion ring (Bouissou et al. 2017 ACS Nano). We also developed a device combining microchannels and pillars and reported that forces are redirected from inwards to outwards with increased cell confinement (Desvignes et al. 2018 Nano Letters).

We showed that the HIV-1 protein Nef modulates the migration of macrophages both in vitro and in vivo, and favors virus dissemination by enhancing the mesenchymal migration and by modulating podosome structure and function (Vérollet et al. 2015 Blood). In addition, we observed that osteoclasts are productively infected by HIV-1. The virus strongly alters podosome organization in osteoclasts, leading to enhanced bone resorption activity (Raynaud-Messina et al. 2018 PNAS USA). These observations likely explains macrophage accumulation in several tissues of HIV-1 infected patients and why they suffer from osteolysis. Macrophages are also the main host cells for Mycobacterium tuberculosis (Mtb). In the context of tuberculosis, we reported that macrophage mesenchymal migration is enhanced, and associated with an accumulation of Mtb-permissive macrophages in lungs (Lastrucci et al. 2015 Cell Research). More recently, we showed that, in tuberculosis microenvironment, the formation of tunneling nanotubes (TNT) by macrophages is increased. When these macrophages are subsequently infected by HIV-1 the virus spread between cells using TNT and the lectin Siglec-1/CD169. These mechanisms could explain how tuberculosis enhances HIV-1 pathogenesis in co-infected patients (Souriant et al., 2019 Cell Rep; Dupont et al., 2020 eLife).  

Main Publications

Dupont M et al. (2020). Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages. Elife 30;9.

Souriant S et al. (2019). Tuberculosis boosts HIV-1 production by macrophages through IL-10/STAT3-dependent tunneling nanotube formation. Cell Rep 26(13):3586-99

Raynaud-Messina B et al. (2018). The bone degradation machinery of osteoclasts: a novel HIV-1 target that contributes to bone loss. Proc Natl Acad Sci USA 115(11):2556-65

Gui P et al. (2018). The protease-dependent mesenchymal migration of tumor-associated macrophages is a novel target in cancer immunotherapy. Cancer Immunol Res 6(11):1337-51

Desvignes E et al. (2018). Nanoscale forces during confined cell migration. Nano Lett 10;18(10):6326-33

Bouissou A et al. (2017). Podosome force generation machinery: a local balance between protrusion at the core and traction at the ring. ACS Nano 11(4):4028-40

2022

Han M, Woottum M, Mascarau R, Vahlas Z, Verollet V, Benichou S. Mechanisms of HIV-1 cell-to-cell transfer to myeloid cells. J Leuk Biol, in press

Jasnin M, Hervy J, Balor S, Bouissou A, Proag A, Voituriez R, Schneider J, Mangeat T, Maridonneau-Parini I, Baumeister W, Dmitrieff S, Poincloux R. Elasticity of dense actin networks produces nanonewton protrusive forces. Nat Commun, in press

2021

Pires D, Calado M, Velez T, Mandal M, Catalao MJ, Neyrolles O, Lugo-Villarino G, Vérollet C, Azevedo-Pereira JM, Anes E. Modulation of Cystatin C in human macrophages improves anti- mycobacterial immune responses to Mycobacterium tuberculosis infection and co-infection with HIV. Frontiers in Immunology 18;12:742822

Bagayoko S, Leon-Icaza SA, Pinilla M, Hessel A, Santoni K, Péricat D, Bordignon PJ, Moreau F, Eren E, Boyancé A, Naser E, Lefèvre L, Berrone C, Iakobachvili N, Metais A, Rombouts Y, Lugo-Villarino G, Coste A, Attrée I, Frank DW, Clevers H, Peters PJ, Cougoule C, Planès R, Meunier E. Host phospholipid peroxidation fuels ExoU-dependent cell necrosis and supports Pseudomonas aeruginosa-driven pathology. PLoS Pathog 17(9):e1009927

2020

Guérit D, Marie P, Morel A, Maurin J, Verollet C, Raynaud-Messina B, Urbach S, Blangy A. Primary myeloid cell proteomics and transcriptomics: importance of beta tubulin isotypes for osteoclast function. J Cell Science (2020) Apr 7.

Genoula G, Marín Franco JL, Maio M, Dolotowicz B, Ferreyra M, Milillo MA, Mascarau R, Moraña EJ, Palmero D, Fuentes F, López B, Barrionuevo P, Neyrolles O, Cougoule C, Lugo-Villarino G, Vérollet C, Sasiain MdC, Balboa L. Fatty acid oxidation of alternatively activated macrophages prevents foam cell formation, but Mycobacterium tuberculosis counteracts this process via HIF-1 activation. Plos Pathogens (2020) Oct 1;16(10)

Marín Franco JL, Genoula M, Corral D, Duette G, Ferreyra M, Maio M, Dolotowicz MB, Aparicio-Trejo OE, Metais A, Patiño-Martínez E, Fuentes F, Soldan V, Moraña EJ, Palmero D, Ostrowski M, Schierloh P, Sánchez-Torres C, Hernández-Pando R, Pedraza-Chaverri J, Rombouts Y, Layre E, Hudrisier D, Vérollet C, Maridonneau-Parini I, Neyrolles O, Sasiain MdC, Lugo-Villarino GC*, Balboa L*. Host-derived lipids from tuberculosis pleurisy impair macrophage microbicidal-associated metabolic activity. Cell Reports (2020) 33(13):108547

2019

2018

Colado A, Genoula M, Cougoule C, Marín Franco JL, Almejún MB, Risnik D, Kviatcovsky D, Podaza E, Elías EE, Fuentes F, Maridonneau-Parini I, Bezares FR, Fernandez Grecco H, Cabrejo M, Jancic C, Sasiain MDC, Giordano M, Gamberale R, Balboa L, Borge M. Effect of the BTK inhibitor ibrutinib on macrophage- and γδ T cell-mediated response against Mycobacterium tuberculosis. Blood Cancer J. (2018) 8(11):100

Desvignes E, Bouissou A, Laborde A, Mangeat T, Proag A, Vieu C, Thibault C, Maridonneau-Parini I*, Poincloux R*. Nanoscale forces during confined cell migration. Nano Letters (2018) 10;18(10):6326-6333

Gui P, Ben-Neji M, Belozertseva E, Dalenc F, Franchet C, Gilhodes J, Labrousse A, Bellard E, Golzio M, Poincloux  R, Maridonneau-Parini I*, Le Cabec V*. The protease-dependent mesenchymal migration of tumor-associated macrophages is a novel target in cancer immunotherapy. Cancer Immunol. Res. (2018) 6(11):1337-1351

Baschieri F, Dayot S, Elkhatib N, Ly N, Capmany A, Schauer K, Betz T, Matic Vignjevic D, Poincloux R, Montagnac G. Clathrin-coated plaques are frustrated endocytosis structures that assemble in response to stiff substrates and serve as signalling platforms to promote sustained Erk activity and cell proliferation. Nature Communications (2018) 9(1):3825

Lugo-Villarino G, Troegeler A, Balboa L, Lastrucci C, Duval C, Mercier I, Benard A, Capilla F, Al Saati T, Poincloux R, Kondova I, Verreck F, Cougoule C, Maridonneau-Parini I, Sasiain MC, Neyrolles O. The C-type lectin receptor DC-SIGN has an anti-inflammatory role in human M(IL-4) macrophages in response to Mycobacterium tuberculosis. Front. Immunol. (2018) 9:1123

Gonçalves-De-Albuquerque CF, Rohwedder I, Ribeiro Silva A, Silveira Ferreira A, Kurz ARM, Cougoule C, Klapproth S, Eggersmann T, Dutra Silva J, Pena de Oliveira G, Luiza Capelozzi V, Gutfilen Schlesinger G, Rijo Costa E, de Cassia Elias Estrela Marins R, Mocsai A, Maridonneau-Parini I, Walzog B, Rocco PRM, Sperandio M, Caire Castro-Faria-Neto H. The yin and yang of tyrosine kinase inhibition during experimental polymicrobial sepsis. Front. Immunol. (2018) 9:901

Cougoule C, Lastrucci C, Guiet R, Mascarau R, Meunier E, Lugo-Villarino G, Neyrolles O, Poincloux R*, Maridonneau-Parini I*. Podosomes, but not the maturation status, determine the protease dependent 3D migration in human dendritic cells. Front. Immunol. (2018) 9:846

Bouissou A, Proag A, Portes M, Soldan V, Balor S, Thibault C, Vieu C, Maridonneau-Parini I*, Poincloux R*. Protrusion Force Microscopy: A Method to Quantify Forces Developed by Cell Protrusions. JoVE (2018) 16;(136)

Genoula M, Marín-Franco JL, Dupont M, Kviatcovsky D, Milillo A, Schierloh P, José Moraña E, Poggi S, Palmero D, Mata-Espinosa D, González-Domínguez E, León-Contreras JC, Barrionuevo P, Rearte B, Córdoba Moreno MO, Fontanals A, Crotta Asis A, Gago G, Cougoule C, Neyrolles O, Maridonneau-Parini I, Sánchez-Torres C, Hernández-Pando R, Vérollet C, Lugo-Villarino G, Sasiain MC, Balboa L. Formation of Foamy Macrophages by Tuberculous Pleural Effusions is triggered by the IL-10/STAT3 Axis through ACAT up-regulation. Front. Immunol. (2018) 9:459

Métais A, Lamsoul I, Melet A, Uttenweiler-Joseph S, Poincloux R, Stefanovic S, Valière A, Stella A, Burlet-Schiltz O, Zaffran S, Lutz PG, Moog-Lutz C. The Asb2α-Filamin A axis is essential for actin cytoskeleton remodeling during heart development. Circulation Research (2018) 122(6):e34-e48

Raynaud-Messina B, Bracq L, Dupont M, Souriant S, Usmani SM, Proag A, Pingris K, Soldan V, Thibault C, Capilla F, Al Saati T, Gennero I, Jurdic P, Jolicoeur P, Davignon JL, Mempel TR, Benichou S, Maridonneau-Parini I*, Verollet C*. The bone degradation machinery of osteoclasts:a novel HIV-1 target that contributes to bone loss. PNAS USA (2018) 115(11):E2556-E2565

Dupont M, Souriant S, Lugo-Villarino G, Maridonneau-Parini I*, Vérollet C*. Tunneling nanotubes: intimate communication between myeloid cells. Front. Immunol. (2018) 9:43

Cervero P, Wiesner C, Bouissou A, Poincloux R, Linder S. Lymphocyte-specific protein 1 regulates mechanosensory oscillation of podosomes and actin isoform-based actomyosin symmetry breaking. Nature Communications (2018) 9(1):515

Lopez-Lopez N, Ramos Martinez AG, Garcia-Hernandez M, Hernandez-Pando R, Castañeda-Delgado J, Lugo-Villarino G, Cougoule C., Neyrolles O, Rivas-Santiago B, Valtierra-Alvarado M, Rubio-Caceres M, Enciso-Moreno J, Serrano CJ. Type-2 Diabetes alters the basal phenotype of human macrophages and diminishes their capacity to respond, internalise and control Mycobacterium tuberculosis. Memórias do Instituto Oswaldo Cruz. (2018) 113(4):e170326

2017

Bouissou A, Proag A, Bourg N, Pingris K, Cabriel C, Balor S, Mangeat T, Thibault C, Vieu C, Dupuis G, Fort E, Lévêque-Fort S, Maridonneau-Parini I, Poincloux R. Podosome force generation machinery: a local balance between protrusion at the core and traction at the ring. ACS Nano (2017) PMID:28355484

Troegeler A, Mercier I, Cougoule C, Pietretti D, Colom A, Duval C, Vu Manh TP, Capilla F, Poincloux R, Pingris K, Nigou J, Rademann J, Dalod MY, Verreck FAW, Al Saati T, Lugo-Villarino G, Lepenies B, Hudrisier D, Neyrolles O. C-type lectin receptor DCIR modulates immunity to tuberculosis by sustaining type I interferon signaling in dendritic cells. PNAS USA (2017) PMID:28069953

Negash A, Mangeat T, Labouesse S, Giovannini H, Belkebir K, Chaumet P, Sandeau N, Poincloux R, Bouissou A, Sentenac A. Super-resolution using speckle illumination microscopy. Mathematics in Imaging Conference paper.  Imaging and Applied Optics (2017) MTh1C. 2

Demy DL, Tauzin M, Lancino M, Le Cabec V, Redd M, Murayama E, Maridonneau-Parini I, Trede N, Herbomel P.  Trim33 / Tif1-γ is essential for macrophage and neutrophil mobilisation to developmental or inflammatory cues.  J Cell Sci. (2017) 130(17):2797-2807

2016

Proag A, Bouissou A, Vieu C, Maridonneau-Parini I, Poincloux R. Evaluation of the force and spatial dynamics of macrophage podosomes by multi-particle tracking. Methods (2016) PMID:26342257

2015

Lastrucci C, Bénard A, Balboa L, Pingris K, Souriant S, Poincloux R, Al Saati T, Rasolofo V, González-Montaner P, Inwentarz S, Moraña E, Kondova I, Verreck FAW, Sasiain MC, Neyrolles O*, Maridonneau-Parini I,*, Lugo-Villarino G and Cougoule C. Tuberculosis is associated with expansion of a motile, permissive and immunomodulatory CD16+ monocyte population via the IL-10/STAT3 axis. Cell Research (2015) PMID:26482950

Vérollet C, Le Cabec V, Maridoneau-Parini I. HIV-1-infection of T lymphocytes and macrophages affects their migration via Nef. Front. Immunol. (2015) PMID:26500651

Vérollet C, Souriant S, Raynaud-Messina B, Maridonneau-Parini I. HIV1 drives the migration of macrophages. Med Sci (2015)PMID:26340831

Proag A, Bouissou A, Mangeat T, Voituriez R, Delobelle P, Thibault C, Vieu C, Maridonneau-Parini I, Poincloux R. Working together: Spatial synchrony in the force and actin dynamics of podosome first neighbors. ACS Nano (2015) PMID: 25791988

Medina I, Cougoule C, Drechsler M, Bermudez B, Koenen RR, Sluimer J, Wolfs I, Döring Y, Herias V, Gijbels M, Bot I, de Jager S, Weber C, Cleutjens J, van Berkel TJ, Sikkink KJ, Mócsai A, Maridonneau-Parini I, Soehnlein O, Biessen EA. Hck/Fgr kinase deficiency reduces plaque growth and stability by blunting monocyte recruitment and intraplaque motility. Circulation (2015) PMID: 26068045

Alvarez-Zarate J, Matlung HL, Matozaki T, Kuijpers TW, Maridonneau-Parini I, van den Berg TK. Regulation of Phagocyte Migration by Signal Regulatory Protein-Alpha Signaling. PLoS One (2015) PMID:26057870

Balboa L, Barrios-Payan J, González-Domínguez E, Lastrucci C, Lugo-Villarino G, Mata-Espinoza D, Schierloh P, Kviatcovsky D, Neyrolles O, Maridonneau-Parini I, Sánchez-Torres C, Sasiain MD, Hernández-Pando R. Diverging biological roles among human monocyte subsets in the context of tuberculosis infection. Clin Sci (Lond) (2015) PMID:25858460

Lastrucci C, Baillif V, Behar A, Al Saati T,  Dubourdeau M, Maridonneau-Parini I and Cougoule C. Molecular and cellular profiles of the resolution phase in DAMP-mediated peritonitis and revelation of leukocyte persistence in peritoneal tissues. Faseb J (2015) PMID: 25609430

Verollet C, Souriant S, Bonnaud E, Jolicoeur P, Raynaud-Messina B, Kinnaer C, Fourquaux I, Imle A, Benichou S, Fackler O, Poincloux R, Maridonneau-Parini I. HIV-1 reprograms the migration of macrophages. Blood (2015) PMID: 25527710

2014

Labernadie A, Bouissou A, Delobelle P, Balor S, Voituriez R, Proag A, Fourquaux I, Thibault C, Vieu C, Poincloux R*, Charrière GM* andMaridonneau-Parini I*. Protrusion Force Microscopy reveals oscillatory force generation and mechanosensing activity of human macrophage podosomes . Nature Communications (2014) PMID:25385672

Maridonneau-Parini I. Control of macrophage 3D migration: a therapeutic challenge to limit tissue infiltration. Immunol Rev. (2014)PMID:25319337

Gui P, Labrousse A, Van Goethem E, Besson A, Maridonneau-Parini I, Le Cabec V. Rho/ROCK pathway inhibition by CDK inhibitor p27kip1 participates in the onset of macrophage 3D-mesenchymal migration. J. Cell Sci. (2014) PMID:25015295

Troegeler A, Lastrucci C, Duval C, Tanne A, Cougoule C, Maridonneau-Parini I, Neyrolles O and Lugo-Villarino G. An efficient siRNA-mediated gene silencing in primary human monocytes, dendritic cells & macrophages. Immulogy & Cell Biology (2014) PMID:24890643

Maridonneau-Parini I. Podosomes are disrupted in PAPA syndrome. Inside Blood. Blood (2014) PMID:24764557

Wiesner C, Le-Cabec V, El Azzouzi K, Maridonneau-Parini I, Linder S. Macrophage migration and matric degradation in 2D and 3D settings. Cell Adhesion and Migration (2014) PMID:24713854

Gouzy A, Larrouy-Maumus G, Bottai D, Levillain F, Dumas A, Wallach JB, Caire-Brandli I, de Chastellier C, Wu TD, Poincloux R, Brosch R, Guerquin-Kern JL, Schnappinger D, Sório de Carvalho LP, Poquet Y, Neyrolles O. Mycobacterium tuberculosis exploits asparagine to assimilate nitrogen and resists acid stress during infection. PLoS Pathog. (2014) PMID:24586151

Park H, Dovas A, Hanna S, Lastrucci C, Cougoule C, Guiet R, Maridonneau-Parini I, Cox D. Tyrosine phosphorylation of WASP by Hck regulates macrophage function. J Biol Chem. (2014) PMID:24482227

2013

Ben Amara A, Gorvel L, Baulan K, Derain-Court J, Buffat C, Vérollet C, Textoris J, Ghigo E, Bretelle F, Maridonneau-Parini I, Mege JL. Placental macrophages are impaired in chorioamnionitis, an infectious pathology of the placenta. J Immunol. (2013) PMID:24163411

Vérollet C, Gallois A, Dacquin R, Lastrucci C, Pandruvada S, Ortega N, Poincloux R, Behar B, Cougoule C, Lowell C, Al Saati T, Jurdic P and Maridonneau-Parini I. Hck contributes to bone homeostasis by controlling the recruitment of osteoclast precursors FASEB J. (2013) PMID: 23742809

Bochet L, Lehuédé C, Dauvillier S, Wang YY, Dirat B, Laurent V, Dray C, Guiet R, Maridonneau-Parini I, Le Gonidec S, Couderc B, Escourrou G, Valet P, Muller C. Adipocyte-derived fibroblasts promote tumor progression and contribute to the desmoplastic reaction in breast cancer. Cancer Res. (2013) PMID:23903958

Marchetti M, Capela D, Poincloux R, Benmeradi N, Auriac MC, Le Ru A, Maridonneau-Parini I, Batut J, Masson-Boivin C. Queusosine biosynthesis is required for sinorhizobium meliloti-induced cytoskeletal modifications on HeLa cells and symbiosis with Medicago truncatula. PLoS One. (2013) PMID:23409119

2012

Bouchet J, Vérollet C, Herate C, Guenzel C, Jarviluoma A, Mazzolini J, Guenzel C, Rafie S, Chames P, Baty D, Saksela K, Niedergang N,Maridonneau-Parini I and Benichou S. Single-domain antibody-SH3 fusions for efficient neutralization of HIV-1 Nef functions. J. Virol. (2012) PMID: 22345475

Maridonneau-Parini I and Cougoule C. Mechanisms of macrophage migration in 3D-environments.Encyplopedia of Inflammatory Diseases Springer Edition (2012)

Cougoule C, Van Goethem E, Le Cabec V, Lafouresse F, Dupré L, Mehraj V, Mège JL, Lastrucci C, Maridonneau-Parini I. Blood leukocytes and macrophages of various phenotypes have distinct abilities to form podosomes and migrate in 3D environments. Eur. J. Cell Biol. (2012) PMID: 22999511

Guiet R, Vérollet C, Lamsoul I, Cougoule C, Poincloux R, Labrousse A, Calderwood DA, Glogauer M, Lutz PG, Maridonneau-Parini I. Macrophage mesenchymal migration requires podosome stabilization by Filamin A. J. Biol. Chem. (2012) PMID:22334688

Ariel A, Maridonneau-Parini I, Rovere-Querini P, Levine JS, Mühl H. Macrophages in inflammation and its resolution. Front Immunol. (2012) PMID:23125842

2011

Villarino GC, Vérollet C, Maridonneau-Parini I and Neyrolles O. Macrophage polarization: convergence point targeted by Mycobacterium tuberculosis and HIV. Front. Immun. (2011) PMID: 22566833

Labrousse A, Meunier E, Record J, Labernadie A, Beduer A, Vieu C, Ben Safta T and Maridonneau-Parini I. Frustrated phagocytosis on micro-patterned immune complexes to characterize lysosome movements in live macrophages. Front. Immun. (2011) PMID: 22566841

Le Cabec V, Van Goethem E, Guiet R and Maridonneau-Parini I. La migration des phagocytes : tour d’horizon. Médecine et Sciences (2011) PMID: 22192751

Vérollet C, Charrière GM, Labrousse A, Cougoule C, Le Cabec V and Maridonneau-Parini I. Extracellular proteolysis in macrophage migration: Losing grip for a breakthrough. Eur. J. Immunol.(2011) PMID: 21953638

Guiet R, Van Goethem E, Cougoule C, Balor S, Valette A, Al Saati T, Lowell CA, Le Cabec V and Maridonneau-Parini I. The process of macrophage migration promotes matrix metalloproteinase-independent invasion by tumour cells. J. Immunol. (2011) PMID: 21880978

Van Goethem E, Guiet R, Balor S, Charrière GM, Poincloux R, Labrousse A, Maridonneau-Parini I and Le Cabec V. Macrophage podosomes go 3D. Eur. J. Cell Biol. (2011) PMID: 20801545

Botella H, Peyron P, Levillain F, Poincloux R, Poquet Y, Brandli I, Wang C, Tailleux L, Tilleul S, Charrière GM, Waddell SJ, Foti M, Lugo-Villarino G, Gao Q, Maridonneau-Parini I, Butcher PD, Castagnoli PR, Gicquel B, de Chastellier C, Neyrolles O. Mycobacterial p(1)-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe. 2011 PMID: 21925112

2010

Labernadie A, Thibault C, Vieu C, Maridonneau-Parini I and Charriere GM. Dynamics of podosome stiffness revealed by atomic force microscopy. Proc.Natl. Acad. Sci USA (2010) PMID: 21081699

Vérollet C, Zhang Y-M, Le Cabec V, Mazzolini J, Charrière G, Labrousse A, Bouchet J, Medina I, Biessen E, Niedergang F, Benichou S, andMaridonneau-Parini I. HIV-1 Nef triggers the formation of multinucleated giant macrophages in a Hck and protease-dependent manner. J. Immunol (2010) PMID: 20488787

Cougoule C, Le Cabec V, Poincloux R, Saati TA, Mège JL, Tabouret G, Lowell CA, Laviolette-Malirat N and Maridonneau-Parini I. Three-dimensional migration of macrophages requires Hck for podosome organization and extracellular matrix proteolysis. Blood (2010) PMID: 19897576 
Highlighted in Research highlights, Nature Rev Mol Cell Biol (2010) 11(4):231

Van Goethem E, Poincloux R, Gauffre F, Maridonneau-Parini I and Le Cabec V. Matrix architecture dictates 3D migration modes of human macrophages: differential involvement of proteases and podosome-like structures. J. Immunol. (2010) PMID: 20018633